DISCUSSION

This study refines and extends previous work in demonstrating that most outbreaks classified as having an undetermined aetiology have clinical characteristics resembling those of outbreaks caused by known agents [Reference Hall2]. In particular, a high proportion of these outbreaks appeared to be consistent with norovirus during the time of the study. The specificity estimates for the profiles ranged from 94% to 98%, suggesting a high degree of confidence in the assignment of a profile to an outbreak. The lower range of sensitivity estimates for the profiles suggest that many of the outbreaks that remained unclassified were probably also associated with known agents. In particular, the norovirus-like clinical profile accounted for 54% of the outbreaks originally classified as of undetermined aetiology, despite the fact that the norovirus-like profile had the lowest estimated sensitivity (70%). Although this estimate was based on a small number of outbreaks, the results are consistent with a recent evaluation of the role of norovirus in foodborne outbreaks reported to CDC from 1998 to 2000 [Reference Turcios10]. Turcios and colleagues found that clinical criteria for classifying outbreaks of norovirus had a specificity of 99% and a sensitivity of 68% [Reference Turcios10]. Thus, our estimate for the proportion of outbreaks attributable to norovirus is probably too low. In addition, recent improvements in the diagnostic capacity of state public health departments mean that a much greater proportion of norovirus outbreaks are now likely to be laboratory confirmed [Reference Turcios10]. Thus, it would not be appropriate to apply the 54% factor from 1982 to 1997 to the current outbreak situation.

Results of this study demonstrate the importance of determining the aetiological agent to assist in the environmental investigation of an outbreak in a restaurant. In practice, there is considerable variability in how EHS determine that a particular food-handling problem represents a contributing factor to the occurrence of a foodborne outbreak. In outbreaks where an agent is already known, the EHS may go into the investigation with predetermined knowledge about what the contributing factors are likely to be. Thus, they will be looking for, and as a result may be more likely to find, a contributing factor that corresponds to the aetiology. Our findings suggest that this is a common practice in outbreak investigations. For example, in 84% of outbreaks caused by C. perfringens, improper holding times and temperatures were identified as contributing factors. This finding is consistent with the fact that improper holding is necessary for sufficient growth of C. perfringens to reach explosively infectious levels on the contaminated food item. In contrast, Shigella has a lower infectious dose and humans are the only source of contamination. Thus, improper holding would not be expected to contribute to outbreaks of Shigella, and in fact it was identified in only 15% of Shigella outbreaks, whereas, poor personal hygiene was identified in 69% of them. Interestingly, improper holding, inadequate cooking, poor personal hygiene and contaminated equipment all appeared to be important for transmission of Salmonella. This finding is consistent with the multiple possible sources for contamination, environmental persistence, and relatively low infectious dose for Salmonella infection.

Our results suggest that EHS use information about the aetiology of an outbreak to guide their evaluations of restaurants. It has not previously been clear how EHS identify contributing factors in outbreaks when no agent is confirmed by laboratory testing. In investigations where the aetiology of the outbreak is truly unknown, the EHS may act as an impartial reviewer of the situation, without selectively focusing on any particular food-handling practices. In this type of investigation, the EHS will probably observe common food-handling problems and may observe the actual problems that led to the occurrence of the outbreak. However, without any knowledge of the aetiology, the EHS may not be able to distinguish one from the other and will either report all observations or none of them. For example, a baseline survey of retail food-handling practices conducted by the Food and Drug Administration found high rates of food-handling errors during routine evaluations [11]. Improper holding times and temperatures were noted in 63% of observations made in full service restaurants and poor personal hygiene practices were noted in 53%. Without knowledge of a specific agent, such observations could be assumed to be contributing to the occurrence of an outbreak. In fact, these were also the most common contributing factors cited in our study for outbreaks of undetermined aetiology that did not match an epidemiological profile. However, improper holding times and temperatures were cited in only 30% and poor personal hygiene in only 20% of these unclassified outbreaks. This suggests reluctance by EHS to identify contributing factors when the relationship between the observed food-handling problem and the aetiology cannot be determined.

Furthermore, in outbreaks of unknown aetiology in which the clinical information suggests an aetiology, our results demonstrate that EHS empirically use this information to guide their evaluations. Thus, outbreaks with diarrhea-toxin and vomiting-toxin profiles were more likely to have improper holding identified as a contributing factor than were outbreaks that remained unclassified. Furthermore, outbreaks with a norovirus-like clinical profile were less likely to have improper holding identified as a contributing factor. In the same manner, outbreaks with a norovirus-like clinical profile were more likely to have poor personal hygiene identified as a contributing factor than were the unclassified outbreaks. These data demonstrate that biologically plausible factors were attributed based on probable aetiology in the absence of laboratory evidence. In contrast, outbreaks matching Salmonella-like or E. coli-like clinical profiles were similar to the unclassified outbreaks with respect to contributing factors identified, consistent with the fact that the biology of these organisms does not lead to a strong a priori hypothesis about the probable source.

These findings have three important implications for outbreak investigations and surveillance. First, the use of clinical profiles is important in guiding environmental evaluations of establishments involved in outbreaks. Identifying a probable aetiology can help narrow the focus of the investigation to better identify the source and the environmental antecedents leading to its occurrence. This is a critical step in improving prevention measures. While unbiased observations of food-handling errors in an outbreak setting may identify many targets for remediation, the failure to focus on the specific problem that led to the occurrence of the outbreak may leave the restaurant at greater risk for recurrence of a similar event. The EHS-Net, a collaborative network of EHS from CDC and nine states, in association with FoodNet, conducted outbreak and non-outbreak environmental evaluations in restaurants to provide a systematic framework for understanding these events. Although pathogen-specific contributing factors were identified, outbreak and non-outbreak restaurants were similar with respect to many characteristics [Reference Hedberg12]. Second, by identifying agents for which specialized laboratory testing may be needed, the use of clinical profiles may help guide diagnostic testing and thus enable laboratory confirmation of the agent. This can also potentially lead to the identification of new and emerging pathogens. Third, and most importantly, clinical profiles of outbreaks can usually be obtained by interviewing cases within hours of initial notification. Thus, this information can be rapidly used to guide investigations, often well before laboratory results are available. Given the importance of rapidly and effectively responding to outbreaks of foodborne disease, this is a major consideration.

While results of this study suggest that EHS are using clinical profiles to guide outbreak investigations in restaurants, it is also clear that relevant contributing factors are less likely to be identified in these outbreaks than in the corresponding outbreaks for which an agent is confirmed by laboratory testing. This suggests either that the use of clinical profiles is not as widespread as it could be, or that there is less confidence in reporting results based on these findings. More widespread use of simple clinical profiles, such as those defined in Table 2, may promote the timeliness and efficiency of outbreak investigations. Presenting data based on clinical profiles in surveillance summaries will provide state and local agencies with an incentive to incorporate these methods and report their results.

Improving the basis for relating contributing factors to suspected aetiology should also provide an incentive to improve reporting of contributing factor data. In 1998, the national foodborne disease surveillance reporting form, containing five contributing factors, was replaced with a much more detailed form including 14 factors that related to contamination of foods, five factors associated with survival or lack of inactivation, and 12 factors associated with proliferation and amplification [Reference Bryan, Guzewich and Todd13]. Improved ascertainment of aetiology and contributing should strengthen the public health system's contribution to safeguarding the food supply.