Risk factors for Campylobacter spp. colonization in French free-range broiler-chicken flocks at the end of the indoor rearing period

The aim of this cross-sectional survey was to identify risk factors for Campylobacter spp. colonization in French free-range broiler flocks at the end of the indoor rearing period (between 35 and 42 days old). Seventy-three broiler farms were studied from March 2003 to March 2004 in France. A questionnaire was administered to the farmers and samples of fresh droppings were taken to assess the flocks'Campylobacter status by bacteriology. Campylobacter species were determined by PCR. A logistic regression analysis was used to assess the influence of various factors on flocks'Campylobacter status. 71.2% of the sampled flocks excreted Campylobacter spp. before going out on the range. The risk of a flock being colonized with Campylobacter was increased in the spring/summer period (RR=1.8, p=0.02) and autumn (RR=2.2, p=0.02) compared to winter, on total freedom rearing farms (RR=3.3, p=0.04) in comparison with farms with a fenced run, when the first disinfection of the poultry-house was performed by the farmer (RR=2.4, p=0.04) instead of a hygiene specialist, when rodent control was carried out by a contractor (RR=1.8, p<0.01) and not by the farmer and when the farmer came into the house twice a day as opposed to three time a day or more (RR=1.5, p=0.02). Use of a specific gate for chick placement decreased the risk of a flock being colonized with Campylobacter (RR=0.5, p=0.01) in comparison with using the gate for manual disposure or the door of the change room.     

Prevalence and risk factors for Salmonella spp. contamination in French broiler-chicken flocks at the end of the rearing period

A nation-wide survey was carried out in 370 randomly chosen French commercial broiler chicken flocks from October 2005 to September 2006 to determine Salmonella spp. prevalence and to identify risk factors for contamination, at the end of the rearing period. The Salmonella status of the flocks was assessed from five faecal samples (litter swabs) analysed by classical bacteriological methods. A flock with at least one contaminated sample was classified as a Salmonella-positive flock. The apparent prevalence of Salmonella was 8.6% (95% CI: 5.7, 11.5%). The most prevalent serovar was S. hadar followed by S. anatum and S. mbandaka. Logistic regression methods were used to analyse the associations between husbandry practices, farm characteristics, general hygiene and the Salmonella status of the sample. The risk for Salmonella contamination of the flock at the end of the rearing period increased when neighbours helped in the placement of day-old chicks. On the contrary, the risk decreased when mobile equipment was dismantled before cleaning and disinfection, when the farm had a specific container for dead-bird disposal and when acetic acid was added to the drinking water.     

Risk factors for Salmonella enterica subsp. enterica contamination in French broiler-chicken flocks at the end of the rearing period.

Broiler-chicken are often Salmonella carriers. However, these bacteria are responsible for major food-borne human infection, in which poultry-meat products are frequently implicated. In order to prevent Salmonella spread during the slaughtering process, control measures should be implemented at the farm level to reduce the prevalence before slaughtering. The objective of this study was to identify the risk factors for Salmonella contamination in French commercial broiler flocks at the end of the rearing period. A prospective study was carried out in 1996 and 1997 on 86 broiler flocks located in western France. The Salmonella status of the flocks was assessed by means of litter swabs and dust samples analyzed with classical bacteriological methods. Sixty flocks (70%) had at least one contaminated environmental sample and were classified as Salmonella-contaminated flocks. Logistic regression was used to assess association of managerial practices, general hygiene and results of environmental Salmonella recovery, with the odds that the flock itself would be Salmonella-contaminated at the end of the rearing period. Salmonella contamination of the house before placing day-old chicks and the Salmonella contamination of day-old chicks were significantly related to Salmonella contamination of the flock at the end of the rearing period. The risk for Salmonella contamination of the flock was increased when feed trucks parked near the entrance of the change room and when feed meal, instead of small pellets, was provided at the start.     

Risk factors for Salmonella enterica subsp. enterica contamination in French broiler-chicken flocks at the end of the rearing period

Broiler-chicken are often Salmonella carriers. However, these bacteria are responsible for major food-borne human infection, in which poultry-meat products are frequently implicated. In order to prevent Salmonella spread during the slaughtering process, control measures should be implemented at the farm level to reduce the prevalence before slaughtering. The objective of this study was to identify the risk factors for Salmonella contamination in French commercial broiler flocks at the end of the rearing period. A prospective study was carried out in 1996 and 1997 on 86 broiler flocks located in western France. The Salmonella status of the flocks was assessed by means of litter swabs and dust samples analyzed with classical bacteriological methods. Sixty flocks (70%) had at least one contaminated environmental sample and were classified as Salmonella-contaminated flocks. Logistic regression was used to assess association of managerial practices, general hygiene and results of environmental Salmonella recovery, with the odds that the flock itself would be Salmonella-contaminated at the end of the rearing period. Salmonella contamination of the house before placing day-old chicks and the Salmonella contamination of day-old chicks were significantly related to Salmonella contamination of the flock at the end of the rearing period. The risk for Salmonella contamination of the flock was increased when feed trucks parked near the entrance of the change room and when feed meal, instead of small pellets, was provided at the start.     

Risk factors for Campylobacter spp. infection in Senegalese broiler-chicken flocks

Our objective was to identify the risk factors for Campylobacter infection in Senegalese broiler flocks. Seventy broiler farms were studied around Dakar from January 2000 to December 2001 around Dakar. A questionnaire was administered to the farmers, and samples of fresh droppings were taken to assess the flocks' Campylobacter status. About 63% of the flocks were infected by Campylobacter spp.; Campylobacter jejuni was the most-prevalent species (P < 0.05). An elevated risk of Campylobacter infection was associated with other animals (mainly laying hens, cattle and sheep) being bred in the farm, the farm staff not wearing their work clothing exclusively in the poultry houses, uncemented poultry-house floors and the use of cartons that transport chicks from the hatchery to the farm as feed plates (rather than specifically designed feed plates). Alternatively, thorough cleaning and disinfection of poultry-house surroundings and manure disposal outside the farm were associated with decreased flock risk.     

Prevalence of and risk factors for Campylobacter colonisation in broiler flocks at the end of the rearing period in France

1. A study was conducted to estimate the prevalence and quantification by species of Campylobacter infection in broiler flocks at the end of the rearing period and to identify associated risk factors.

2. A questionnaire about the rearing period was completed and caecal samples were collected from 121 broiler flocks in Brittany, France, during 2008.

3. Campylobacter was isolated in 87 out of 121 flocks – a prevalence of 71.9% (95% CI, 63.7–80.1%), including 40.5% of Campylobacter jejuni and 29.8% of Campylobacter coli.

4. The average concentration, in positive flocks, was 7.96 log₁₀ cfu/g and ranged from 3.15 to 10.32 log₁₀ cfu/g.

5. The average concentration by species was: 7.57 log₁₀ cfu/g for C. jejuni and 8.44 log₁₀ cfu/g for C. coli.

6. There was a seasonal effect, with increased risk of Campylobacter colonisation in June, July and August (odds ratio (OR) = 9.59, 95% CI 1.15–79.75).

7. The other factors, associated with lower risk of Campylobacter colonisation, were the acidification of drinking water (OR = 0.33, 95% CI 0.13–0.86), antibiotic treatment at the beginning of the rearing period (OR = 0.20, 95% CI 0.07–0.55) and rodent control around the house (OR = 0.18, 95% CI 0.03–0.95).

8. The results show that hygiene practices and biosecurity measures could lead to a reduction in Campylobacter colonisation.     

Risk factors for Campylobacter spp. colonization in broiler flocks in Iceland

We sampled 1091 Icelandic broiler flocks at slaughter from May 2001 to December 2003 to determine the prevalence of, and investigate risk factors for the presence of, Campylobacter spp. at the flock level. Approximately 15% of the flocks were positive for Campylobacter spp.; most (95%) of the infected flocks being raised during the months of April–September. Based on the data from the latter months, and using multivariable logistic regression with random effects for herd, we found that the odds of a flock being positive for Campylobacter spp. increased with age and flock size. Additionally, vertical ventilation systems were strongly associated with positive flocks (OR = 5.3). After controlling for these variables, we found no evidence of an effect of: year; company; Campylobacter being carried over from one flock to the next; time interval between flocks; using (at the hatcheries) eggs laid on the floor; density of bird housing, or the number of catch lots a flock was divided into for slaughtering purposes on the risk of a Campylobacter-positive flock.     

Risk factors for the presence of Campylobacter spp. in Dutch broiler flocks

The campylobacter status of 495 broiler flocks sampled in The Netherlands between April 1997 and December 2000 was related to farm- and flock-specific information obtained from questionnaires to identify potential risk factors for campylobacter presence. Approximately 30% of the flocks tested positive for Campylobacter spp. in at least one pooled faecal sample. Multivariable logistic regression showed significant risk increments for: ages 29-35 days (OR = 2.34) and 36-42 days (OR = 3.96) compared to 22-28 days; > or =5 broiler houses on the premises (OR = 3.02); the presence of other farm animals on the farm (OR = 1.88); the presence of animals on farms within 1 km (OR = 9.56); and summer (OR = 3.48) and fall (OR = 2.59) compared to winter. Furthermore, hatcheries differed (ORs from 5.42 to 20.2), although this variable showed strong collinearity with the variables explaining feed mill and integrated poultry operations. We also identified interaction in which an increased risk from children entering the broiler house (OR = 28.0) was diminished by the use of broiler-specific workclothes. Population attributable fractions (PAFs) suggested that animals on farms within 1 km (PAF = 0.76) and hatchery (PAF = 0.67) had the highest impacts on campylobacter presence in Dutch broiler flocks. These factors, however, lack an easy interpretation of the mechanism behind the suggested effect.     

Temperature-related risk factors associated with the colonization of broiler-chicken flocks with Campylobacter spp. in Iceland, 2001-2004

Our objective was to identify temperature-related risk factors associated with the colonization of broiler-chicken flocks with Campylobacter spp. in Iceland, with an underlying assumption that at minimum ambient temperatures, flies (Musca domestica) play a role in the epidemiology and seasonality of Campylobacter. At slaughter, pooled caecal samples were obtained from 792 flocks that hatched between March 15 and September 15 each year from 2001 to 2004, and cultured for Campylobacter. Daily temperature data (average, maximum and minimum temperatures) were obtained from the Icelandic Meteorological Office. We determined the closest weather station to each farm using ArcGIS 9. We then used logistic-regression models (with a random-effects term for farm) to examine associations between flock positivity and temperature-related predictors. The overall prevalence of Campylobacter was 27.4%, and the month with the highest prevalence (54.4%) was August. The final model included cumulative degree-days (CDD) above an average temperature of 4.4 degrees C and the presence of 1 or more days below a maximum temperature of 8.9 degrees C (threshold below which fly activity was expected to be substantially reduced and egg laying was not expected to occur) during the period 2-4 weeks (i.e. days 8-28) before slaughter. Below 79 CDD, the risk of flock Campylobacter colonization was generally low. Between 79 and 139 CDD, the risk increased gradually, but was lower for flocks raised during periods with 1 or more days <8.9 degrees C than flocks raised without days <8.9 degrees C. The risk increased sharply under conditions of high CDD (>139) and when the maximum temperature remained >8.9 degrees C during the period 2-4 weeks before slaughter.     

Colonization of broilers with Campylobacter in conventional broiler-chicken flocks

Eight of 16 conventional broiler-chicken flocks examined contained Campylobacter. All isolates were identified as C. jejuni except from 1 flock were C. coli was isolated. One herd consisting of 6 different houses where Campylobacter regularly has been isolated was continuously examined. It was not possible to isolate Campylobacter from newly hatched chickens or from environmental samples and cloacal swabs during the 2 first weeks of growth.     

Risk factors for Salmonella enterica subsp. enterica infection in senegalese broiler-chicken flocks

Our objective was to assess the association of managerial practices, general hygiene and Salmonella infection in Senegalese broiler flocks. Seventy broilers farms were studied from January 2000 to December 2001 around Dakar. A questionnaire was submitted to the farmers and samples of fresh broiler droppings were taken. A 28.6% of the flocks were infected by Salmonella (mainly Hadar and Brancaster serovars). Salmonella infection of the previous flock (OR=6.82) and of day-old chicks (OR=3.73), frequent poultry farmers’ visits (OR=5.38) and keeping sick birds inside the farm (OR=5.32) increased the risk of Salmonella infection. But, using antibiotics on day-old chicks (OR=0.17) and a detergent for cleaning (OR=0.16) decreased the risk.     

Risk factors for Listeria monocytogenes contamination in French laying hens and broiler flocks

The objective of this study was to identify potential risk factors for Listeria monocytogenes contamination in French poultry production. Eighty-four flocks of layer hens kept in cages and 142 broiler flocks were included in this study. For each production type, a questionnaire was submitted to farmers and fecal samples were taken to assess the L. monocytogenes status of the flocks during a single visit to the farm. Two logistic regression models (specific to each production) were used to assess the association between management practices and the risk of L. monocytogenes contamination of the flock. The prevalence of L. monocytogenes-positive flocks was 30.9% (95% CI: 21.0; 40.9) and 31.7% (95% CI: 24.0; 39.4) for cage-layers and broiler flocks, respectively. For layer flocks, the risk of L. monocytogenes contamination was increased when pets were present on the production site. When droppings were evacuated by conveyor belt with deep pit storage, the risk of L. monocytogenes contamination decreased significantly. Feed meal was found to be associated with a higher risk of L. monocytogenes contamination than feed crumb. For broiler flocks, the risk of L. monocytogenes contamination was increased when farmers did not respect the principle of two areas (clean and dirty) at the poultry house entrance. A first disinfection by thermal fogging and the absence of pest control of the poultry house before the arrival of the next flock was found to increase the risk of contamination. When litter was not protected during storage and when farm staff also took care of other broiler chicken houses, the risk of L. monocytogenes contamination increased significantly. In the case of the watering system, nipples with cups were found to decrease the risk of contamination.     

Risk factors for Campylobacter colonization in broiler flocks in Japan

The present study was conducted to estimate the prevalence of and to identify the risk factors for Campylobacter colonization in broiler flocks in Japan. Campylobacter colonization status in flock was evaluated by culturing pooled caecal excrement from 124 broiler flocks. Potential exposure to risk factors was evaluated with a questionnaire for the broiler producers. Odds ratios (ORs) were calculated using a multivariable logistic regression analysis. The prevalence of Campylobacter-positive flocks was 43.5% (upper and lower limits of 95% confidence interval (CI(95%) ): 34.8, 52.3). Multivariable logistic regression model identified two variables as risk factors for Campylobacter colonization. The ORs of Campylobacter colonization were higher in flocks in western Japan (OR=2.68; CI(95%) : 1.04, 6.91) than in eastern Japan, and in flocks supplied with undisinfected drinking water (OR=7.41; CI(95%) : 3.11, 17.66) than in those supplied with disinfected drinking water. These findings indicate that water may play an important role in Campylobacter colonization in broiler flocks in Japan and the use of disinfected water may reduce the risk of Campylobacter colonization.     

Risk factors for Salmonella persistence after cleansing and disinfection in French broiler-chicken houses

A prospective survey was carried out in 86 broiler houses in western France to identify risk factors for Salmonella persistence in French broiler houses. The Salmonella status of the house after cleansing and disinfection, was assessed from gauze-swab samples taken from the walls, feeders, ventilation system and bedding (analysed with classical bacteriological methods). Thirty three (38%) houses had at least one contaminated sample and were classified as Salmonella-contaminated houses in the logistic regression. The absence of a terminal disinfection and a disinfection procedure performed by the farm staff rather than a contractor were positively related to the Salmonella contamination of the house after cleansing and disinfection. The risk for Salmonella persistence after decontamination was increased if rodents were observed by the farmer, if a large part of the access area to the house was accessible to trucks, and if a disease leading to a treatment occurred in the previous flock.     

Campylobacter spp. in broiler flocks at farm level and the potential for cross-contamination during slaughter

Screening of broiler flocks for their Campylobacter carriage on farm level and consequently the spread of Campylobacter spp. during slaughtering can help to identify hygiene control points. Therefore, between December 2001 and August 2002 in total 51 broiler flocks from three farms of different geographical regions in Germany were analysed for thermophilic Campylobacter. Campylobacter spp. were isolated from 45% of the broiler flocks examined. Subsequently, 1101 samples were taken from 22 flocks during different stages of processing. Samples were collected from: transport crates before and after cleaning/disinfection, evisceration, post-scalded and post-chilled carcasses and endproducts. Additionally, 45 selected Campylobacter isolates of droppings were genotyped by pulsed-field gel electrophoresis (PFGE). Campylobacter carriage of flocks showed seasonal variation, with the highest contamination rate during the period of June to August. No evidence was found for a horizontal transmission from one broiler flock to the next via a persistent house-contamination. In each positive flock, one to three different genotypes were found. One or two clones dominated isolations obtained from the farm level. The fact that in different flocks indistinguishable isolates of clonal origin were detected during the same rearing period suggested a transmission between the broiler flocks or an intermittent common external source. In one case, isolates of clonal origin were detected in various farms during different rearing periods. Sampling during processing confirmed that the entrance of a positive flock resulted in contamination of the abattoir environment. Campylobacter spp. were isolated from all sampling stages along the processing line, with a percentage of 91.1-100 of isolates at different stages of slaughtering.     

Campylobacter spp. in conventional broiler flocks in Northern Ireland: epidemiology and risk factors

Risk factors for Campylobacter infection in conventional broiler flocks in the time period up to the first removal of birds to slaughter were investigated over a maximum of five consecutive production cycles in a cohort of 88 broiler farms in Northern Ireland. Samples for Campylobacter culture, which consisted of 14 cloacal swabs per flock, were collected from one house on each farm prior to the first depopulation of birds. In total 388 flocks were sampled, of which 163 tested positive for Campylobacter spp. (42.0%; 95% CI 35.1–48.9%).

Data on farm and flock variables were obtained from questionnaires and random-effects logistic regression modelling used to investigate the association between these and the Campylobacter status of flocks. Six variables, all of which were significant at p < 0.05, were included in the final multivariable model. These included a combined variable on the presence of rodents on farms, which showed an increased odds of infection in flocks where the farmer reported having observed rodents during the production cycle (OR = 2.1) and/or where rodent droppings were observed at the sampling visit (OR = 2.9). Other variables that were significantly associated with an increased odds of infection included the age of the birds at sampling (odds ratio for its linear effect = 1.16 for each day of increase in age), season (summer versus other seasons OR = 2.0), farms with three or more broiler houses (OR = 2.9 compared to those with one house), the frequency of footbath disinfectant changes (OR = 2.5 for once weekly and OR = 4.0 for less than once weekly compared to twice weekly changes) and a categorical variable on the standard of tidiness and cleanliness of the broiler house ante-room (OR = 2.0 and OR = 4.9 for flocks from houses with poorer standards). There was no significant evidence of direct carry-over of infection from one production cycle to the next, neither was there evidence of other farm species acting as a source of infection.     

Risk factors for Campylobacter colonisation during rearing of broiler flocks in Great Britain

We investigated the associations between Campylobacter colonisation and management practices and farm characteristics in 603 housed broiler batches originating from 137 farms in Great Britain. All study batches were the initial batch slaughtered from the selected house on enrolled farms. Between 1 and 15 batches were sampled from each farm throughout the study. A total of 34.2% of the batches was Campylobacter positive and multivariable multilevel logistic regression revealed that the risk of Campylobacter colonisation was highest in July (OR = 3.4, CI_95%:1.8; 6.4), August (OR = 3.4, CI_95%:1.9; 6.2) and September (OR = 3.7, CI_95%:1.9; 7.1). Cattle on or adjacent to the farm increased the risk (OR = 1.7, CI_95%:1.1; 2.7), whereas chlorinated drinking water reduced it (OR = 0.5, CI_95%:0.2; 0.9). If the first removed batch from the previous flock in the house had been Campylobacter positive, the first batch of the following flock was also more likely to be colonised (OR = 3.2, CI_95%:2.1; 4.9). This association was more likely due to a persistent risk practice or source of Campylobacter on the farm than a direct carry-over from previous flock.     

Prevalence and risk factors for Campylobacter spp. in chicken broiler flocks in Reunion Island (Indian Ocean)

Our objectives were to determine Campylobacter prevalence in broiler chicken flocks in Reunion Island and to define specific practices associated with the presence of Campylobacter spp. Infection in Reunionese broiler flocks. Fifty broiler flocks were studied in Reunion Island from May 2007 to February 2009. A questionnaire was submitted to the farmers and samples of fresh droppings were collected to assess the flock's Campylobacter status. Fifty four percent of the flocks were infected by Campylobacter spp.: 30% (95% CI: 28.71-31.29) were infected with Campylobacter coli and 17% (95% CI: 15.95-18.05) with Campylobacter jejuni; only 7% (95% CI: 6.28-7.72) were infected by both species at the same time. Several poultry houses in the farm (OR=11.2; [1.05-92]) and cleaning without any detergent (OR=13.1; [2.1-78.3]) increased the risk of Campylobacter infection. A distance higher than 500 m between broiler farms (OR=0.27; [0.1-0.8]) and use of disinfectant during the rearing period decreased this risk of infection (OR=0.15; [0.1-0.75]).     

Prevalence and risk factors for Salmonella spp. and Campylobacter spp. caecal colonization in broiler chicken and turkey flocks slaughtered in Quebec, Canada

We conducted an observational study to estimate prevalence and risk factors for Salmonella spp. and Campylobacter spp. caecal colonization in poultry. Eighty-one broiler chicken and 59 turkey flocks selected among flocks slaughtered in the province of Quebec, Canada, were included in the study. Flock status was evaluated by culturing pooled caecal contents from about 30 birds per flock. Exposure to potential risk factors was evaluated with a questionnaire. Odds ratios were computed using multivariable logistic regression.

The prevalence of Salmonella-positive flocks was 50% (95% CI: 37, 64) for chickens and 54% (95% CI: 39, 70) for turkeys, respectively. Odds of Salmonella colonization were 2.6 times greater for chicken flocks which failed to lock the chicken house permanently. In turkeys, odds of Salmonella colonization were 4.8–7.7 times greater for flocks which failed to be raised by ≤2 producers with no other visitors allowed onto the premises, or origin from a hatchery.

The prevalence of Campylobacter-positive flocks was 35% (95% CI: 22, 49) for chickens and 46% (95% CI: 30, 62) for turkeys. Odds of colonization were 4.1 times higher for chicken flocks raised on farms with professional rodent control and 5.2 times higher for flocks with manure heap >200 m from the poultry house, and also increased with the number of birds raised per year on the farm and with the age at slaughter. For turkeys, odds of Campylobacter flock colonization were 3.2 times greater in flocks having a manure heap at ≤200 m from poultry house and 4.2 times greater in flocks drinking unchlorinated water.     

Dynamics of Campylobacter spp. spread investigated in 14 broiler flocks in Switzerland

Ten conventional and four extensive outdoor broiler flocks, distributed over nine farms, were investigated twice per week during a 35-58-day rearing period to observe the dynamics of Campylobacter spp. spread within these flocks. Strains isolated during this period were genotyped by restriction fragment length polymorphism analysis of the flaA gene and macrorestriction profiling with pulsed field gel electrophoresis. A total of 4112 samples were collected; 157 (3.8%) of these samples were Campylobacter positive, with all C. jejuni. The positive samples were distributed over three conventional and two extensive outdoor flocks on five farms. These five positive flocks were colonized from the fifth to the seventh week of age and remained colonized until slaughter. Each of the flocks showed a flock-specific genotype of Campylobacter that predominated until slaughter. Presuming different ways of entry, a combination of this fact and the observed dynamics of C. jejuni spread within the flocks indicates that a single source from the environment may have been responsible for the colonization of each flock. These conclusions may serve to further develop combat strategies at farm level.