Review article
Campylobacters as zoonotic pathogens: A food production perspective

https://doi.org/10.1016/j.ijfoodmicro.2007.01.006Get rights and content

Abstract

Campylobacters remain highly important zoonotic pathogens worldwide which infect an estimated 1% of the population of Western Europe each year. Certain campylobacters are also important in infections of animals, particularly of the reproductive tract, and some are involved in periodontal disease. This paper focuses, however, on the two species which are most important in food-borne infections of humans, Campylobacter (C.) jejuni and C. coli. Infection with these campylobacters is serious in its own right but can also have long-term sequelae such as reactive arthritis and Guillain–Barré syndrome. The pathogens are ubiquitous in nature and in domestic animals and, as a consequence, are found frequently in the environment and on many raw foods, of both plant and animal origin and bacterial numbers can be very high on certain key foods like raw poultry meat. Although all commercial poultry species can carry campylobacters, the risk is greater from chicken because of the high levels of consumption. Campylobacters are relatively ‘new’ zoonotic pathogens as routine culture from clinical specimens only became possible in the late 1970s. As a consequence there is much that still needs to be understood about the behaviour and pathogenicity of these highly important bacteria. In particular, and from a food industry/food safety perspective, it is important to better understand the behaviour of C. jejuni and C. coli in the food production environment, and how this affects their ability to survive certain food production processes. There is a belief that campylobacters are much more sensitive to hostile conditions than either salmonellas or Escherichia coli. Much of data to support this view have been derived from laboratory experiments and may not fully represent the natural situation. Studies are showing that campylobacters may be more robust than previously thought and thus may represent a greater challenge to food safety.

We recommend that research is undertaken to better understand how campylobacters behave in the food chain and how responses to relevant conditions affect their ability to survive processing and their virulence. There is also a need to better understand the reasons why campylobacters are capable of frequent change, particularly in the expression of surface antigens.

Introduction

The family Campylobacteriaceae comprises small (0.2–0.9 μm wide and 0.2–5.0 μm long), spiral formed (Fig. 1), Gram-negative bacteria with 18 species, six sub-species and two biovars (Table 1). They are very different from other pathogens associated with food-borne disease in that they are essentially microaerophilic, growing best in an atmosphere containing approximately 10% CO2 and approximately 5% O2. The species pathogenic for man also have a rather narrow temperature range for growth with a maximum temperature of ∼ 46 °C and a minimum of 30 °C. These are classed as thermophilic campylobacters.

Table 1 shows the current members of the family Campylobacteriaceae. They are found in a wide range of sites in animals with some causing infections of the reproductive tract of certain domestic species which can lead to either abortion and/or infertility. Others are mainly involved in periodontal diseases. Campylobacters are principally known, however, as zoonotic pathogens. Most infections are caused by Campylobacter jejuni and C. coli although in the developing world C. upsaliensis is also important. C. jejuni and C. coli present an interesting dilemma. They can cause severe disease in infected people (see Epidemiology section) but are carried in the intestinal tracts of all types of domestic livestock and many wild animals, almost always without any harmful effects. This carriage does have major consequences for human health in terms of food-borne disease. The differences in pathogen behaviour in man and in animals are not yet fully understood but are likely to be due to differential bacterial gene expression in different hosts.

Campylobacters are the leading cause of bacterial diarrhoeal disease worldwide, although data are not yet available to allow an estimate of the contribution of these bacteria to all bacterial infections. The World Health Organization (WHO) estimates that ∼ 1% of the population of Western Europe will be infected with campylobacters each year. This estimate is supported by data from England and Wales (Wheeler et al., 1999), which found that for each reported case of campylobacter infection there were approximately nine others that were not reported. In England and Wales in 2004 there were ∼ 50,000 cases reported. Assuming that the estimate of Wheeler et al. (1999) is correct, the true total is around 450,000, close to that suggested by WHO data. There are similarly high incidences throughout the developed world, but for unknown reasons the incidence is particularly high in New Zealand.

The infectious dose for campylobacters is low at a few hundred cells (Anonymous, 2005). Infection can have an incubation period of 1–10 days with most people exhibiting clinical symptoms by 4 days. It is characterised by profuse, often bloody diarrhoea, particularly in children, acute abdominal pain and fever. In the UK it has been reported that 82% of people admitted to hospital with a diagnosis of ‘food poisoning’ were suffering from campylobacter infection (Adak et al., 2002). Most cases recover after a period of bed rest. As with other enteric infections maintenance of fluid balance is important.

Treatment with antibiotics for uncomplicated campylobacter infection is rarely indicated. However, antimicrobial resistance to clinically important drugs used for treatment (especially macrolides and fluoroquinolones) is increasingly reported for campylobacters. There is evidence that patients infected with antibiotic-resistant strains suffer worse outcomes (invasive illness or death) than those infected with sensitive strains (Helms et al., 2005). This underlines the need to limit the use of antimicrobials in veterinary and medical clinical practice to limit the occurrence of resistance. In a small percentage of cases, long-term and potentially serious complications can arise. Infection with C. jejuni is the most common predisposing factor to the peripheral neuropathies Guillain–Barré (GBS) and Miller Fisher Syndromes. Not all strains of C. jejuni seem capable of causing these sequelae and there are differences in those associated with the two syndromes (Takahashi et al., 2005). This is considered in greater detail later in this review.

This review will provide information on the epidemiology of campylobacters in human infection and food animal production. Potential control measures in chicken production are discussed in some detail as are possible post-processing treatments. Details are also provided on the behaviour of these pathogens in environments relevant to food production and how this might affect food safety.

We are aware that members of the genus Arcobacter are becoming increasingly recognised as zoonotic pathogens and that they have many behaviours and environmental niches in common with campylobacters. A definitive link between arcobacters and human disease has not yet been established but concern has been raised over their presence in meat and dairy products and over recent evidence suggesting that the genus Arcobacter, especially A. butzleri, may be involved in human enteric disease. The distinctive feature differentiating arcobacters from campylobacters is the ability of the former to grow at 15 °C. Various aspects of arcobacters as potential food-borne pathogens have recently been reviewed by Lehner et al. (2005). This report concentrates on campylobacters but it is reasonable to assume that processes which control these bacteria in foods are likely to be equally successful against arcobacters.

Section snippets

Disease burden

The disease burden has been described in several different ways. In the US, it has been estimated that food-borne campylobacters infect around 2.5 million people each year (Mead et al., 1999). In England and Wales, estimates show that there were approximately 360,000 cases of food-borne campylobacter infection in 2000, accounting for 27% of all food-borne disease (Adak et al., 2002). In The Netherlands there are an estimated 80,000 cases per year (de Wit et al., 2001) and the attributable cost

Traditional methods

Many methods for isolating campylobacters from clinical specimens have been published and Bolton et al. (1997) showed that they can be isolated from human faecal samples using microaerobic–atmosphere-generating systems. With foods enrichment is usually required. The broth used affects recovery (Baylis et al., 2000) and the sampling method affects the numbers recovered (Jørgensen et al., 2002). The time to confirm the presence of campylobacters in food and environmental samples can exceed

Campylobacters in primary food production

All animals used for food can be campylobacter-positive as can many companion species (domestic pets). Samples from the natural environment, such as groundwater (Schaffner et al., 2004), will also frequently contain these pathogens. The Schaffner study reports the presence of campylobacters in groundwaters of mainly mountainous regions. The authors concluded that these organisms multiply in a natural way in the environment or that they are able to survive for a long time. The greatest current

Food processing control measures

Generally speaking, foods are made safe through inactivation, e.g. heat treatment, and/or through inhibition of growth to prevent multiplication of pathogens to harmful levels. However, since campylobacters remain a concern even at low levels, their presence in foods at the point of consumption must be prevented, so growth inhibition is not relevant as a method of control. Compared to other pathogenic bacteria campylobacters are relatively heat sensitive so commercial heat processes set within

Campylobacters in domestic and commercial kitchens

The World Health Organization (WHO) has outlined five keys to safer food. They are:

  • Keep clean

  • Separate raw and cooked

  • Cook thoroughly

  • Keep food at safe temperatures

  • Use safe water and raw materials

This applies also to campylobacters and raw foods like poultry will continue to be sources of these in household kitchens and commercial catering. Such foods must therefore at all times be recognised as presenting a risk if not adequately cooked, or if they come into contact with ready-to-eat foods. It

Discussion

This report has discussed extremely important zoonotic, food-borne pathogens, campylobacters, which worldwide infect millions of people each year. Infection, particularly in children, can be severe and in this group bloody diarrhoea is a common feature. Infection can also have debilitating long-term sequelae, causing substantial morbidity and placing a major cost burden on national health care systems. Most cases are caused by C. jejuni and this pathogen is unusual in that general outbreaks are

Acknowledgements

ILSI Europe and the Emerging Microbiological Issues Task Force would like to thank the authors of this report, Tom Humphrey, Sarah O'Brien and Mogens Madsen, as well as its scientific reviewer Eric Bolton, Regional Health Protection Laboratory (UK) for the preparation of this article.

This work was commissioned by the Emerging Microbiological Issues Task Force of the European branch of the International Life Sciences Institute (ILSI Europe). Industry members of this task force are bioMérieux

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