Poultry as a reservoir for foodborne disease - News & Features

24 April 2014
Poultry as a reservoir for foodborne disease

This article by Frieda Jorgensen and Caroline Willis first appeared in Microbiologist Vol 15 No. 1, March 2014.

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Poultry and poultry products are recognized as the most significant source of human Campylobacter and Salmonella infections in the developed world, including the UK. Outbreak investigations and case-control studies investigating risk-factors and transmission routes have identified poultry meat and eggs as major sources of infection. However, non-foodborne routes such as animal contact, and occupational or recreational exposure, are also important.

Salmonella Rates 1993-2012

Poultry meat, and chicken liver or duck liver products were implicated as the source in 62 of 103 Campylobacter outbreaks reported to the Health Protection Agency (HPA) between 2000 and 2012. Eggs and poultry meat were implicated in 52 and 43 Salmonella outbreaks (of 382 in total reported to the HPA), respectively, over the same time period. In the EU, eggs and egg products were one of the main food vehicles associated with foodborne outbreaks, while broiler meat was the fifth most frequent cause of foodborne Salmonella outbreaks in 2008 (EFSA, 2010a). Moreover, data from the European Commission’s Rapid Alert System for Food and Feed (2008) indicated that reports of microbiological contamination in poultry meat were more common than for any other food type. In an EU survey from 2008, raw chicken meat was frequently contaminated with campylobacters (approximately 80% of samples) but less so with salmonellas (approximately 16%) (EFSA, 2010b).

Campylobacter human cases 2003-2012

The extent to which different infection risk factors are associated with different sources can be inferred by combining case-control studies with source attribution studies (i.e., studies that determine the predisposition of specific genotypes to infect particular animals). Such studies have provided further evidence that poultry is the major source of campylobacteriosis.

Chicken Production and Slaughter

The introduction of microbiological criteria in legislation and EU targets for reducing Salmonella in broiler flocks has contributed to a decline in flock prevalence of this organism in some member states (EFSA, 2013), with only 3.2% of broiler flocks being positive for Salmonella in 2011. The UK Salmonella National Control Programme (NCP) has particularly focused on two serovars (Salm. Enteritidis and Salm. Typhimurium), but this has been accompanied by a general reduction in salmonellosis in the UK (Figure 1). Salmonella is now very rarely detected in UK broiler flocks. Only four broiler flocks in 2012 tested positive for Salm. Typhimurium out of a total of approximately 38,000 flocks tested, and none were positive for Salm. Enteritidis. There is no similar specific legislation for campylobacters in raw chicken meat, but authorities and industry in EU countries have introduced measures aimed at reducing Campylobacter contamination from farm to fork. However, in the UK the large majority of chicken flocks have tested positive at slaughter for campylobacters in recent years despite the introduction of stricter biosecurity measures.

Chicken flocks are usually colonized with Campylobacter as a result of environmental exposure but may show no signs of ill health when colonized, although bird health indicators have been associated with the likelihood of a flock being colonized. In most European countries, including the UK, chicken flocks are more likely to be colonized in the summer months possibly due to increased infection risks (Lawes et al., 2012). Although poultry that are farmed outdoors may appear to be more at risk of becoming exposed and colonized there is no evidence that Salmonella is more prevalent in poultry farmed outdoors compared with housed birds. In contrast, campylobacters appear to be more prevalent in poultry farmed with access to range compared with housed birds.

Slaughter, plucking and evisceration, in particular, lead to carcass contamination and a significant proportion of carcasses will have high levels of campylobacters when a positive flock is slaughtered. In comparison, slaughter of cattle, pigs and sheep/lamb is associated with much lower levels of carcass contamination despite these animals also demonstrating high colonization rates (EFSA, 2013), probably due to a slaughter process that limits cross-contamination from gut material to the carcass.

Compared with the numbers found on poultry meat and liver surfaces, bacterial numbers inside tissues are low but nonetheless may be significant when undercooking occurs. Campylobacter can be present inside liver and meat tissue, although most infections are thought to relate to Campylobacter cells on the surface. In one study, 30 chicken livers were examined with campylobacters being detected in 27 and 2 had internal counts of more than 1,100 CFU/100 g. An increased number of Campylobacter outbreaks have been observed in recent years, and many of these have been linked to the consumption of chicken or duck liver pâtés and parfaits where the livers had been inadequately cooked. Campylobacters can also be present inside chicken breast fillets (approximately 20%) but at very low levels (an average of 15 cells/100 g in positive fillets has been reported).

Until the late 1990s, it was common practice to add antibiotics to animal feed, including poultry feed, in order to promote growth of the animals. This practice selectively encourages the growth of antibiotic-resistant bacteria. Thus, the use of enrofloxacin as a growth promoter in poultry has been linked with an increase in ciprofloxacin resistance in campylobacters and salmonellas, whilst the use of avoparcin correlated with an increase in the prevalence of vancomycin-resistant enterococci in chicken meat (Willis, 2000). While a ban on the use of medically important antibiotics as growth promoters was introduced in the EU in 1999, this practice has continued in other parts of the world. Moreover, some studies suggest that the decrease in the use of growth promoters has been accompanied by an increase in the use of prophylactic and therapeutic antibiotics. Therefore, there is a continued risk of pathogenic bacteria in poultry developing antibiotic resistance patterns that may make infections with these organisms very difficult to treat effectively in humans.

Egg Production

Raw shell eggs can be contaminated with Salmonella, either presenting as shell contamination due to contact with faeces after laying (migration of the organism through the shell is possible) or as egg content contamination due to colonization of the hen’s oviduct. Salmonella Enteritidis, in particular, is known to be closely associated with eggs. In the late 1980s, the incidence of Salm. Enteritidis Phage Type (PT) 4 infections increased sharply in the UK and Europe, and this increase was linked with consumption of poultry meat and shell eggs. Studies have indicated that Salm. Enteritidis has a greater ability to persist in the laying hen reproductive tissues and egg contents, compared with other Salmonella types (Van Immerseel, 2010). In 1998, the Lion Quality Scheme was introduced in the UK, setting down a code of practice covering all stages of egg production, and including vaccination of pullets destined for egg-producing flocks against Salm. Enteritidis. Between 1997 and 2000, there was a 54% reduction in Salm. Enteritidis PT4 cases reported in the UK, and this decline has been maintained since then (Figure 1). Salmonella contamination levels in British eggs are now extremely low, with an FSA study in 2003 finding Salmonella in only 0.34% of eggs tested. However, egg-related outbreaks of Salmonella still occur, and these are largely linked with catering eggs produced outside the UK. For example, in 2011, 262 people in the UK were infected with Salm. Enteriditis PT14b. The source of infection was traced to eggs from a specific shed on one farm in Spain, which supplied implicated catering establishments in the UK. It is important to ascertain the proportion of foodborne disease which is linked to imported foods so that the effect of national intervention measures can be assessed.

These figures reflect that only one laying flock tested positive for Salm. Enteritidis and two for Salm. Typhimurium out of 4,042 flocks included in the UK NCP in 2012. However, across the EU 4.2% of laying hen flocks were positive for Salmonella spp. in 2011 causing concerns for imported eggs (EFSA, 2013).

Environmental Transmission

It has been demonstrated that, when raw chicken is handled and prepared in a domestic kitchen, contamination of hands, kitchen surfaces, cloths and equipment with Salmonella and/or Campylobacter frequently occurs (Gorman et al., 2002). Moreover, when contaminated eggs are whisked, aerosols may spread over 40cm away from the mixing point. Contamination was not reliably removed during a laboratory simulation of a typical washing-up process (Mattick et al., 2003). Therefore, there is a considerable risk of cross-contamination from raw chicken and eggs to other ready-to-eat foods that are handled in the kitchen. Of 101 outbreaks in private houses, 44 were associated with poultry and cross-contamination was described as a contributory factor in 28 of these (Ryan et al., 1996).

Future Strategies

In the EU, legislation has contributed to lowering the Salmonella presence in poultry, but some countries still have far to go. The current strategies to further reduce salmonellosis arising from the poultry reservoir require continued efforts on improved egg and broiler meat hygiene supported by vaccination. The current UK Food Standards Agency target for Campylobacter is to reduce the proportion of chicken carcasses with more than 1,000 CFU/g of neck-skin to 10% by 2015 (in 2008, 27% of samples had > 1,000 CFU/g). While control measures applied at the chicken meat processing stage will have no impact on environmental transmission arising from the farm reservoir, interventions such as rapid crust chilling of carcasses can result in significant reductions of the levels of campylobacters on carcasses. The Scandinavian countries have a particularly good record of low pathogen prevalence in poultry, and while differences in climate and livestock density may explain this to an extent, industry practices including all-in-all-out systems within farms and other high-level biosecurity measures also play significant roles. Promising new interventions including fatty fish-based feed additives and novel Campylobacter vaccines exploiting knowledge of glycosylation may help reduce the presence of campylobacters in poultry in the future.


EFSA (European Food Safety Authority) (2010a) Analysis of the baseline survey on the prevalence of Campylobacter in broiler batches and of Campylobacter and Salmonella on broiler carcasses in the EU, 2008, Part A: Campylobacter and Salmonella prevalence estimates. The EFSA Journal 8, 1503.

EFSA (European Food Safety Authority) (2010b) The Community Summary Report on trends and sources of zoonoses and zoonotic agents in the European Union in 2008. The EFSA Journal 8, 1496

EFSA, (European Food Safety Authority), ECDC (European Centre for Disease Prevention and Control). (2013). The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-borne Outbreaks in 2011; EFSA Journal 11:3129.

Willis CL (2000) Antibiotics in the food chain: their impact on the consumer. Reviews in Medical Microbiology 11: 153-160.

Gorman R, Bloomfield S, Adley CC. (2002). A study of cross-contamination of food-borne pathogens in the domestic kitchen in the Republic of Ireland. Int J Food Microbiol. 76:143-150.

Ryan MJ, Wall PG, Gilbert RJ, Griffin M, Rowe B.1996. Risk factors for outbreaks of infectious intestinal disease linked to domestic catering. Commun Dis Rep CDR Rev. 6:R179-183.

Mattick K, Durham K, Domingue G, Jørgensen F, Sen M, Schaffner DW, Humphrey T. 2003. The survival of foodborne pathogens during domestic washing-up and subsequent transfer onto washing-up sponges, kitchen surfaces and food. Int J Food Microbiol. 85:213-226.

Van Immerseel F. 2010 Stress-induced survival strategies enable Salmonella Enteritidis to persistently colonize the chicken oviduct tissue and cope with antimicrobial factors in egg white: A hypothesis to explain a pandemic. Gut Pathog. 2:23.

Lawes JR, Vidal A, Clifton-Hadley FA, Sayers R, Rodgers J, Snow L, Evans SJ, Powell LF. (2012) Investigation of prevalence and risk factors for Campylobacter in broiler flocks at slaughter: results from a UK survey. Epidemiol Infect. 140:1725-1737.

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