A multi-centre prospective case-control study of campylobacter infection in persons aged 5 years and older in Australia

To the Editor: I write in response to the article by Stafford and colleagues [Reference Stafford1] who provide results from a case-control study examining risk factors for sporadic Campylobacter infections in Australia. In their article they report consumption of undercooked chicken to be significantly associated with illness. This is in keeping with findings reported in other case-control studies [Reference Eberhart-Phillips2, Reference Friedman3]. However the risk of illness from consumption of undercooked chicken is likely to be overstated due to the effects of information bias, particularly differential misclassification. A number of factors, including interview and questionnaire design, the characteristics of cooked poultry meat, consumer perceptions on thoroughness of cooking and the physiology of Campylobacter organisms all require consideration before the significance of a relationship between consumption of chicken labelled as being undercooked and illness can be established.

To begin with it would be helpful to know how questions on undercooked chicken were phrased. Some studies attempt to qualify the use of the term undercooking by providing a definition, for example, eating ‘chicken that was pink on the inside’ [Reference Friedman3]. Obviously, in large case-control studies that examine scores of variables, it is difficult to cover all bases in published material. However, the means of elucidating such information is particularly relevant to this study because eating undercooked chicken was identified as the principal independent risk factor (aOR 4·7).

Myoglobin, a protein found in muscle, is the pigment most responsible for the colour of meat [Reference King and Whyte4]. A number of factors including pH levels, meat source, packaging conditions, freezing history, fat content, and preservation treatments contribute to the phenomenon known as ‘pink defect’ seen in well-cooked white meats [Reference King and Whyte4, Reference Holownia, Chinnan and Reynolds5]. Meat pinking and red or bloody poultry parts are critical for consumer rejection as they directly relate to an undercooked appearance of the product [Reference Smith and Northcutt6], with most consumers assessing cooking status by the colour of the meat or its juice [Reference King and Whyte4].

However, from a food safety perspective, a food thermometer is recommended to ensure cooked meats have reached a temperature that will ensure destruction of pathogenic organisms [7]. However, it has only been in the last few years that food safety authorities have moved away from promoting messages such as cooking meat ‘until the inside is no longer pink and the juices run clear’, as well as specifying temperature and time rules and use of food thermometers. The United States Department of Agriculture (USDA) and Food Safety Inspection Service (FSIS) have updated their recommendations for cooking poultry using an extensive health promotion campaign to highlight the inappropriateness of visual assessment and the need to use a food thermometer. Such practices have important implications, with evidence showing colour is not a reliable indicator that organisms have been destroyed or that meat is cooked. On this basis, there can be no confidence in visually inspecting a meat product to ascertain if it is safely cooked, and use of a food thermometer is the most reliable method for guaranteeing the inactivation of foodborne pathogens in cooked meat [Reference King and Whyte4].

The temperature at which different bacteria are destroyed varies, as does the temperature at which different meat and poultry types are deemed to be thoroughly cooked. Campylobacter are generally regarded as being less robust than many other pathogenic bacteria [Reference Rosenquist8], demonstrating particular sensitivity to heat [Reference Park9]. Given Campylobacter has a D value of less than 1 min at 60°C [Reference Keener10] it becomes possible that chicken not cooked to a recommended temperature will still have been exposed to sufficient heat to destroy or inactivate any Campylobacter present. This view is supported by a number of risk-based assessments [Reference Rosenquist8, 11]. If true, the relevance of undercooking should be reconsidered and greater emphasis instead placed on examining the relationship between human infection and cross-contamination and poor hand hygiene, as suggested by the authors in their conclusion.

It is recognized that Campylobacter contamination levels in commercial kitchens are particularly high [Reference Dawkins, Bolton and Hutchinson12]. In this study and others [Reference Eberhart-Phillips2] consumers of undercooked chicken have been shown to have a higher rate of eating chicken in restaurants, and eating in restaurants per se. Because both activities have been associated with increased risk of Campylobacter infection it is possible that reports of undercooking are being confounded by eating at restaurants where it is biologically plausible that cross-contamination is occurring.

In summary the use of a questionnaire or interviews collecting self-reported data on undercooked chicken, while practical, is inappropriate to answer the question of whether consumption of undercooked chicken is a significant risk factor for campylobacteriosis. Evidence shows use of a food thermometer is the only method that can reliably determine thoroughness of cooking. Determining whether meat is cooked based on colour is no longer recommended in the United States, although mixed messages continue from government food authorities in Australia. To label or define undercooked chicken as being ‘pink on the inside’ is also misleading, especially given that ‘meat pinking’ and ‘bone darkening’, are not uncommon in cooked poultry meat. Physiological attributes of the Campylobacter organism may also contribute to undercooking being a less likely explanation of illness. Given the impracticality of direct observation, the inclusion of a subjective assessment of subjects' food handling and food hygiene practices into epidemiological studies examining risk factors may allow a better understanding of the magnitude that undercooking and cross-contamination play in disease transmission.