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Campylobacter jejuni is not merely a commensal in commercial broiler chickens and affects bird welfare.

ABSTRACT: Campylobacter jejuni is the leading cause of bacterial food-borne infection; chicken meat is its main source. C. jejuni is considered commensal in chickens based on experimental models unrepresentative of commercial production. Here we show that the paradigm of Campylobacter commensalism in the chicken is flawed. Through experimental infection of four commercial breeds of broiler chickens, we show that breed has a significant effect on C. jejuni infection and the immune response of the animals, although these factors have limited impact on the number of bacteria in chicken ceca. All breeds mounted an innate immune response. In some breeds, this response declined when interleukin-10 was expressed, consistent with regulation of the intestinal inflammatory response, and these birds remained healthy. In another breed, there was a prolonged inflammatory response, evidence of damage to gut mucosa, and diarrhea. We show that bird type has a major impact on infection biology of C. jejuni. In some breeds, infection leads to disease, and the bacterium cannot be considered a harmless commensal. These findings have implications for the welfare of chickens in commercial production where C. jejuni infection is a persistent problem. Importance: Campylobacter jejuni is the most common cause of food-borne bacterial diarrheal disease in the developed world. Chicken is the most common source of infection. C. jejuni infection of chickens had previously not been considered to cause disease, and it was thought that C. jejuni was part of the normal microbiota of birds. In this work, we show that modern rapidly growing chicken breeds used in intensive production systems have a strong inflammatory response to C. jejuni infection that can lead to diarrhea, which, in turn, leads to damage to the feet and legs on the birds due to standing on wet litter. The response and level of disease varied between breeds and is related to regulation of the inflammatory immune response. These findings challenge the paradigm that C. jejuni is a harmless commensal of chickens and that C. jejuni infection may have substantial impact on animal health and welfare in intensive poultry production:

SUBMITTER: Humphrey S

PROVIDER: S-EPMC4161246 | biostudies-other | 2014 Jul

REPOSITORIES: biostudies-other

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Campylobacter jejuni is not merely a commensal in commercial broiler chickens and affects bird welfare.

Humphrey Suzanne S Chaloner Gemma G Kemmett Kirsty K Davidson Nicola N Williams Nicola N Kipar Anja A Humphrey Tom T Wigley Paul P

mBio 20140701 4

Campylobacter jejuni is the leading cause of bacterial food-borne infection; chicken meat is its main source. C. jejuni is considered commensal in chickens based on experimental models unrepresentative of commercial production. Here we show that the paradigm of Campylobacter commensalism in the chicken is flawed. Through experimental infection of four commercial breeds of broiler chickens, we show that breed has a significant effect on C. jejuni infection and the immune response of the animals, ...[more]

PMID: 24987092

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Project description:Campylobacter jejuni is one of the most prevalent causes of bacterial gastroenteritis worldwide, and it is largely associated with consumption of contaminated poultry. Current Campylobacter control measures at the poultry production level remain insufficient, and hence there is the need for alternative control strategies. We evaluated the potential of the monoterpene (-)-α-pinene for control of C. jejuni in poultry. The antibacterial and resistance-modulatory activities of (-)-α-pinene were also determined against 57 C. jejuni strains. In addition, the anti-quorum-sensing activity of (-)-α-pinene against C. jejuni NCTC 11168 was determined for three subinhibitory concentrations (125, 62.5, 31.25 mg/L) over three incubation times using an autoinducer-2 bioassay based on Vibrio harveyi BB170 bioluminescence measurements. The effects of a subinhibitory concentration of (-)-α-pinene (250 mg/L) on survival of C. jejuni, and in combination with enrofloxacin on fluoroquinolone resistance development in C. jejuni, were determined in a broiler chicken model, by addition of (-)-α-pinene to the broiler water supply. The reduction of C. jejuni numbers by (-)-α-pinene was further determined in broiler chickens that were colonized with either fluoroquinolone-susceptible or -resistant strains, by direct gavage treatment. We observed weak in vitro antimicrobial activity for (-)-α-pinene alone (MIC >500 mg/L), but strong potentiating effects on antibiotics erythromycin and ciprofloxacin against different Campylobacter strains (>512 fold change). After 24 h of treatment of C. jejuni with (-)-α-pinene, its quorum-sensing signaling was reduced by >80% compared to the untreated control. When given in the drinking water, (-)-α-pinene did not show any significant inhibitory effects on the level of C. jejuni in the colonized chickens, and did not reduce fluoroquinolone resistance development in combination with enrofloxacin. Conversely, when (-)-α-pinene was administered by direct gavage, it significantly reduced the number of fluoroquinolone susceptible C. jejuni in the colonized broiler chickens. These results demonstrate that (-)-α-pinene modulates quorum-sensing in Campylobacter, potentiates antibiotics against different Campylobacter strains, and reduces Campylobacter colonization in broiler chickens.

Project description:Background: Campylobacter is commonly transmitted to humans from chickens. Campylobacter jejuni is the species most frequently associated with human illness, and the most prevalent species recovered from poultry. Objective: The objective of this study was to analyse a sub-population of C. jejuni from two broiler flocks on the farm and at slaughter using whole-genome sequencing to gain insights into the changes in the Campylobacter population during broiler production, including changes in virulence and antimicrobial resistance profiles. Methods: In this study, ten composite faecal samples (n=10), obtained by pooling ten fresh faecal samples (n=10), were collected in the broiler house on two farms on days 14, 21, 28, and 34 (n=80) and ten composite (n=10) caecal samples were collected at the time of slaughter for each flock (n=20). These were tested for C. jejuni using the ISO 10272-2:2016 method. Seven isolates were randomly selected from each of the nine Campylobacter-positive sampling points (n=63) and were subjected to antimicrobial susceptibility tests. Their genomes were sequenced and the data obtained was used to characterise the population structure, virulence, antimicrobial resistance determinants and inter-strain variation. Results: The Farm 1 isolates had three MLST types (ST257-257, ST814-661 and ST48-48) while those on Farm 2 were ST6209-464 and ST9401. Interestingly, only the MLST types positive for most of the virulence genes tested in this study persisted throughout the production cycle, and the detection of antimicrobial resistance determinants (gyrA T86I and tetO) increased after thinning and at slaughter, with the detection of new strains. Conclusion: The persistence of the most virulent strains detected in this study throughout the production cycle has important implications for the risk to consumers and requires further investigation. The detection of new strains within the population corresponding with the time of thinning and transportation reflects previous reports and provides further evidence that these activities pose a risk of introducing new Campylobacter strains to broiler batches.

Project description:This study aimed to identify whether early-life conditions in broiler chickens could affect their behavior and welfare, and whether or not this was associated with an altered gut microbiome composition or diversity. Broilers were tested in a 2 x 2 factorial design with hatching conditions [home pen (OH) or at the hatchery (HH)] and enrichment (dark brooder (EE) or no brooder (NE) until 14 days of age) as factors (N = 6 per treatment combination). Microbiota composition was measured in the jejunum on days (d) 7, 14, and 35 and in pooled fecal samples on day 14. A novel environment test (NET) was performed on days 1 and 11, and the behavior was observed on days 6, 13, and 33. On day 35, composite asymmetry was determined and footpad dermatitis and hock burn were scored. In their home pen, HH showed more locomotion than OH (P = 0.05), and NE were sitting more and showed more comfort behavior than EE at all ages (P <0.001 and P = 0.001, respectively). On days 6 and 13 NE showed more eating and litter pecking while sitting, but on day 33 the opposite was found (age*enrichment: P = 0.05 and P <0.01, respectively). On days 1 and 11, HH showed more social reinstatement in the NET than OH, and EE showed more social reinstatement than NE (P <0.05). Composite asymmetry scores were lower for EE than NE (P <0.05). EE also had less footpad dermatitis and hock burn than NE (P <0.001). Within OH, NE had a more diverse fecal and jejunal microbiome compared to EE on day 14 (feces: observed richness: P = 0.052; jejunum: observed richness and Shannon: P <0.05); the principal component analysis (PCA) showed differences between NE and EE within both HH and OH in fecal samples on day 14, as well as significant differences in bacterial genera such as Lactobacillus and Lachnospiraceae (P <0.05). On day 35, PCA in jejunal samples only showed a trend (P = 0.068) for differences between NE vs. EE within the OH. In conclusion, these results suggest that especially the dark brooder affected the behavior and had a positive effect on welfare as well as affected the composition and diversity of the microbiome. Whether or not the behavior was modulated by the microbiome or vice versa remains to be investigated.

Dataset Information

Campylobacter jejuni is not merely a commensal in commercial broiler chickens and affects bird welfare.

Publications

Campylobacter jejuni is not merely a commensal in commercial broiler chickens and affects bird welfare.

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