Are happy chickens safer chickens? Tom Humphrey t.j.humphrey@liverpool.ac.uk Professorial Fellow in Food Safety Science Director NCZR University of Liverpool
Campylobacter as zoonotic pathogens in UK Estimated 700000 cases in 2010 Marked early summer peak Elderly people more at risk Disease is not trivial ~100 deaths; bacteraemia in cancer patients 140 120 100 80 Cases/100k 60 40 20 0-9 20-59 >60 0 An inflamed and ulcerated colon
Hospital admission by age group in England and Wales 100 80 % 60 40 20 0 0-9 20-29 40-49 60-69 80+ Age range People with bowel cancer at particular risk. Bacterial behaviour is like that in a compromised chicken Need to understand the elderly gut 600 500 400 300 200 100 0 Campylobacter mortality by age group 0-9 20-29 40-49 60-69 80+
Genetic gain (% of mean) Chickens have been taken a long way: production systems and welfare directly impact on Campylobacter Rates of genetic change expected in farm livestock 3.5 3 2.5 2 1.5 1 0.5 0 Poultry Pigs Sheep Beef
Contaminated chicken meat is the major vehicle for Campylobacter infection Chicken source of 50-80% of Campylobacter cases ~ 80% carcasses positive at retail Control in chicken production essential to improve public health It is rarely like this
Campylobacter and chicken: two health threats High level surface contamination (10 9 ): A cross-contamination risk Contamination of liver and muscle tissues: Heightened risk from under-cooking (20% muscle +) ~80% of cases chicken-related Many chicken liver paté outbreaks Eating chicken out, a major risk factor
Campylobacter contamination after preparing chickens The traditional view is that the greatest risk to consumers is from cross-contamination Objects % Contaminated Cutting boards 77 Crockery 72 Taps 82 Dishcloths 74 Salt-cellars 60
Intensive slaughter compromises effective control Plants kill ~ 200 birds per minute Designed for economy Frequent bird-to-bird contact Total pathogen removal not possible Thus main focus should be on-farm
We tend to eat chicken produced intensively
Epidemiology of Campylobacter in broilers 797 flocks (27000 caeca) Examined at first depopulation Biosecurity increasingly difficult to sustain Modern broilers highly disease-susceptible Flocks more likely to be positive if: - Fast broilers rather than slow - They are APEC-infected - They have poor gut health (hock/pad burn) Bird growth rate is the major driver in susceptibility to Campylobacter and APEC and regulates the in vivo behaviour of C. jejuni
Does laboratory work mirror the on-farm situation? Laboratory Farm The in vivo behaviour of C. jejuni strongly influenced by the state of the host The ideal conditions under which laboratory animals are kept mean that C. jejuni behaves as a harmless commensal This may not mimic behaviour on-farm On-farm, C. jejuni is rarely alone Poor health and welfare can play a major role in C. jejuni infection on-farm
Animals are victims of their environment
Chickens experience poor welfare but does it matter? Low cost food essential Possible because of intensive production and genetic improvement of farm animals Poor environments, production-associated conditions and endemic/zoonotic disease Are chickens so dumb that their environment doesn t matter? Does the drive for increased production threaten animal welfare? Do unhappy animals pose a greater food safety risk than ones that are happy? If so, what is the nature of the increased threat? Campylobacter will be used as an example
Broiler growth rate has a major influence on bird susceptibility to endemic and zoonotic diseases
Campylobacter: a poorly controlled chicken commensal? Liver T cells of infected birds proliferate on stimulation by C. jejuni Some strains invasive in well chickens Others invade in compromised host Host responds as if Campylobacter is pathogenic Immune responses confine Campylobacter to gut C. jejuni isolated from liver and can cause vibrionic hepatitis (+ other factors) Association with bird health and welfare suggests an opportunistic pathogen Fig 2: Chickens immune responses to campylobacter differ from those to other commensals 1200 1000 800 600 400 IgY titre Camp LAB 200 0 7 28 Days
Campylobacter and broilers: disconnection between productivity and food safety Are modern broilers more Campylobactersusceptible because: Grow more quickly Have poorer gut health More APEC-susceptible Clear link between infections Campylobacter colonises a damaged gut more easily Compromised immune responses Chicken production has not stood still. Data that were relevant 10 years ago less so now
Broiler production compromises immunocompetence and the gut environment
There is a campaign for change
Broilers in higher welfare systems have: Better gut health: lower hock marks and pododermatitis Lower levels of endemic disease: avian pathogenic E. coli (APEC) A better environment: dry litter with a neutral ph Fewer birds that are Campylobacter-positive and less extraintestinal spread Hock marks Pododermatitis
Housed systems and bird type and Campylobacter Longitudinal studies on flocks to compare production systems FF (JA 57)v STD (Cobb 500) FF had lower Campylobacter Much less likely to have APEC Is this bird type, stocking density, 10 diet and/or environment? 0 80 70 60 50 40 30 20 % birds Campylobacter-positive STD FF 1 2 3 4 5 6 7 8 9 % APEC condemnations STD Figure 6: Stocking density and litter ph 9 8 ph 38 kg/m 30 kg/m FF 7 6 5 4 13 25 33 39 Age (days)
100 Ross 308 v Hubbard JA 57 80 60 Campylobacter Levels Hock marks Podo Birds stocked at 30 Kg/M2 40 20 0 Ross 308 JA 57 Camilla Brena 2011
In some chickens, Campylobacter infection is a welfare issue
Broiler genotype, gut health and Campylobacter Poor health and welfare are risk factors for Campylobacter - Hock marks and pododermatitis - APEC and necrotic enteritis In some birds, Campylobacter is a welfare problem - We assumed that hock marks/pododermatitis preceded Campylobacter - Perhaps we were incorrect! - In rapidly-growing birds, C. jejuni causes gut health problems - Raised hock marks and pododermatitis
Infection with C. jejuni caused high levels of pododermatitis in fast-growing birds 40 35 30 25 20 Birds with pododermatitis Control C. jejuni 15 10 5 0 Ross 308 Hubbard JA 57
Extra-intestinal spread by Campylobacter
In vivo behaviour of C. jejuni in chickens is strongly linked to the health and welfare of the host Chickens responses to endemic disease and/or environment important Birds can experience acute stress Change in pathogen behaviour Invasive phenotypes of Campylobacter Can this be mitigated?
OD at 600nm Noradrenaline increases Campylobacter growth rate 1.0 0.8 0.6 0.4 0.2 + NA Cont. Campylobacter numbers higher in animals post-transport Cross-infection common during transport Campylobacter are poor at capturing iron NA increases growth rate and virulence by allowing iron uptake 0.0 Effects much greater than with 0 6 12 18 24 30 36 42 48 Salmonella Rapid growth in iron-restricted environments
C. jejuni pre-treated with noradrenaline is more invasive in chickens 70 % positive 60 50 40 30 20 + NA Cont 10 0 Liver Caeca This models spread from stressed birds
Better controlling endemic diseases of broilers would help to better control Campylobacter
Infection with E. coli is a risk for Campylobacter in broilers and promotes invasive behaviour Avian pathogenic E. coli (APEC) important broiler pathogens Losses average at ~6% of birds (51000000 chickens per year) Multiple presentations Flocks with high levels of APEC infection more likely to have Campylobacter Kirsty Kemmett 2011
Campylobacter and E. coli interact APEC infection is a high risk factors for Campylobacter Extra-intestinal spread of Campylobacter more likely in birds with APEC Less likely with slower growing birds The reverse has been seen in mice and in earlier work in chickens in Germany Identify risk factors for APEC and determine if better control of this infection also helps to control Campylobacter Research in Israel has shown that rapidly growing birds are more susceptible to APEC
Bacteria per field of view Endemic APEC infection and Campylobacter in broilers 6 4 2 0 Campylobacter FISH liver in liver CJ Group A aa CJ + EC Group B Jejunum Link between E. coli and Campylobacter in field High % of Campylobacter+ livers in EC+ flocks Mucosal damage and extra-intestinal spread in lab studies when CJ and EC together No effect when CJ or EC given singly Crosstalk? Link between NE and C. jejuni in Norway Caecum CJ or EC CJ+ EC CJ or EC CJ+ EC High levels in mucosal damage in co-infected birds
The control of Campylobacter in poultry production Control cannot and will not be cost-neutral Biosecurity can reduce flock carriage rates Other interventions are necessary Effects of the production environment on bird health/welfare must be included in the development of host-based controls Essential to better understand host-pathogen interaction and what influences this