A restatement of the natural science evidence base regarding the source, spread and control of Campylobacter species causing human disease.

Food poisoning caused by Campylobacter (campylobacteriosis) is the most prevalent bacterial disease associated with the consumption of poultry, beef, lamb and pork meat and unpasteurized dairy products. A variety of livestock industry, food chain and public health interventions have been implemented or proposed to reduce disease prevalence, some of which entail costs for producers and retailers. This paper describes a project that set out to summarize the natural science evidence base relevant to campylobacteriosis control in as policy-neutral terms as possible. A series of evidence statements are listed and categorized according to the nature of the underlying information. The evidence summary forms the appendix to this paper and an annotated bibliography is provided in the electronic supplementary material.

Introduction

The consumption of food and drink contaminated with Campylobacter bacteria can cause campylobacteriosis in humans. While food may be made safe with adequate cooking, and by avoiding cross-contamination during food preparation, Campylobacter is the most common cause of acute bacterial gastroenteritis both in the UK and globally [1]. Campylobacteriosis is chiefly a sporadic disease with many isolated cases that usually peak in early summer in the UK, though there are occasional larger outbreaks [2]. Most people who become infected with Campylobacter suffer from illness and discomfort and require time to convalesce, but severe disease and death can occur. The use of antibiotics is only recommended for those at greatest risk of severe disease or death from campylobacteriosis (chiefly the young, old and immune compromised). In other patients, antibiotics only shorten the disease by a few days and their prescription may accelerate the evolution of antibiotic resistance, which has already been observed in Campylobacter. The total cost to society of foodborne campylobacteriosis is estimated at over £700 million per annum in the UK alone [3].

A suite of producer, food-chain and public health measures have been implemented to attempt to reduce the levels of campylobacteriosis in the UK, particularly targeting poultry, which has been identified as the main source of human infection. Surveys indicate that levels of Campylobacter in fresh poultry at retail outlets in the UK have decreased in recent years, but reported human Campylobacter infections have remained relatively constant [4]. Further interventions are needed to limit the individual and economic impacts of campylobacteriosis, though each imposes different levels of costs on livestock production, processing and retail sectors. Designing better control measures without unnecessary costs requires a better understanding of the origin and transmission dynamics of the Campylobacter species causing human disease.

The aim of this ‘Restatement' is to present a clear and succinct summary of the evidence for the source and spread of Campylobacter in the food chain and how it might be controlled. We focus on the UK although the evidence base is relevant to many other countries, particularly those in temperate regions. The Restatement is written for an informed but not expert audience, for example, senior policy-makers with food safety in their brief. We also highlight areas where the evidence base is poorly developed to assist policy makers. In a policy area that can be contentious, we aim to be as policy-neutral as possible in the compilation and presentation of evidence.

Material and methods

The relevant literature on Campylobacter was reviewed with particular focus on studies in the UK and a first draft evidence summary was produced by a subset of the authors. At a workshop, all authors met to discuss the different evidence statements and to assign a description of the nature of the evidence to each statement using a restricted set of terms. The statements and their assessments were subsequently debated via correspondence until a consensus was achieved. We use the following restricted terms to describe the evidence, indicated by abbreviated codes, which are similar to those used in previous Restatements.

[S A strong evidence base likely involving multiple experimental studies or field data collections, with appropriate detailed statistical or other quantitative analysis.

[L from perhaps only one or few studies, with further studies needed to strengthen the evidence base.

[E A consensus of expert opinion extrapolating results from related systems and well-established epidemiological and pathological principles.

[P: Projections based on the available evidence for which substantial uncertainty often exists.

Results

The summary of the natural science evidence base relevant to Campylobacter control policy-making in the UK is given in the appendix, with an extensive annotated bibliography provided as electronic supplementary material.

Discussion

The most important source of Campylobacter that cause human disease is meat from farmed animals such as cattle, pigs and particularly broiler chickens. Campylobacter infect the intestines of most farmed animals and are regularly found on fresh carcasses, particularly the carcasses of broiler chickens, and it is likely that bacteria in digestive tracts are spread to carcasses during slaughter and factory processing. Live bacteria on meat and carcasses may be ingested by humans via cross-contamination to other foods and items if food preparation hygiene is poor prior to cooking, or if meat is not cooked sufficiently.

Poultry is the most consumed meat in the UK and a major source of Campylobacter. Campylobacter from non-poultry livestock, particularly ruminants, are also a significant cause of human disease, as is increasingly shown by genetic source-attribution studies including recent studies using whole-genome sequencing [5]. The evidence base for Campylobacter levels on retail beef, lamb and pork, and the effect of food-chain interventions designed to reduce these, is less well developed than for poultry. The Restatement highlights gaps in our knowledge on the efficacy of on-farm and factory processing food-chain interventions aimed at reducing rates of contamination on cattle, pigs and particularly broiler chickens, where further research would be helpful. There has been a decrease in Campylobacter levels on poultry over the last 5 years in the UK but levels of human campylobacteriosis cases have remained static. It is not yet known whether this is due to Campylobacter levels on poultry being a poor measure of risk from consuming poultry meat, an increase in the consumption of chicken, an increase in the number of people over 60 years of age who are more susceptible to Campylobacter, or whether the risks from consuming other meats or becoming infected from non-food sources has increased [4,6].

The Advisory Committee on the Microbiological Safety of Food recommends a multi-prong approach to tackling disease from Campylobacter combining interventions across the entire food system including non-poultry livestock [1]. Our survey of the evidence supports this recommendation as there is no evidence that any single intervention has a major effect, whereas concerted multiple-intervention campaigns in Iceland and New Zealand have had some effect. Nevertheless, to implement more effectively such a ‘multiple-hurdle' strategy, it would be helpful to conduct more whole food-chain studies that robustly quantify the likely main environmental sources of Campylobacter and then go on to analyse the effect of specific on-farm and in-factory interventions on changing the numbers and types of Campylobacter on final food products. Experimental and modelling work that evaluates how different interventions interact and combine across the food-chain to reduce levels on retail products would be particularly valuable [7]. The increasing availability of whole-genome DNA sequencing approaches combined with epidemiological and classic microbiological methods offers new tools to understand Campylobacter origins, transmission and disease (e.g. [7]). Lastly, we need to better understand the behavioural science of how people assess and understand the risks of food poisoning from Campylobacter (and of course other agents), and how they can be empowered to protect themselves and other people.