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5. Risk Assessment of thermophilic Campylobacter spp. in broiler chickens

5.1 Summary of the Risk Assessment

5.1.1 Introduction

An understanding of thermophilic Campylobacter spp., and specifically Campylobacter jejuni in broiler chickens is important from both public health and international trade perspectives. In order to achieve such an understanding, evaluation of this pathogen-commodity combination by quantitative risk assessment methodology was undertaken.

The first steps of this process, hazard identification, hazard characterization and the conceptual model for exposure assessment were presented at an expert consultation in July 2001, and summarized in the report of that consultation.[4] The exposure assessment model described the production-to-consumption pathway for fresh and frozen broiler chicken carcasses prepared and consumed in the home.

The final step, risk characterization, integrates the exposure and dose-response information in order to attempt to quantify the human-health risk attributable to pathogenic thermophilic Campylobacter spp. in broiler chickens. The risk assessment model and results were presented to the present expert consultation in the working document MRA 02/01. Recommendations for modifications and/or areas for further development of the exposure assessment model, arising from the 2001 consultation were taken into consideration and, where possible, were incorporated during preparation of the MRA 02/01 report. Recommendations, that were not incorporated, are noted in the exposure assessment summary section below.

5.1.2 Scope

The purpose of the work was to develop a risk assessment that attempts to understand how the incidence of human campylobacteriosis is influenced by various factors during chicken rearing, processing, distribution, retail storage, consumer handling, meal preparation and finally consumption. A benefit of this approach is that it enables consideration of the broadest range of intervention strategies. The risk characterization estimates the probability of illness per serving of chicken associated with the presence of thermophilic Campylobacter spp. on fresh and frozen whole broiler chicken carcasses with the skin intact and which are cooked in the domestic kitchen for immediate consumption. A schematic representation of the risk assessment is shown in Figure 5.1.

FIGURE 5.1: Schematic representation of the risk assessment of Campylobacter spp. in broiler chickens.

5.1.3 Approach Hazard identification

Thermophilic Campylobacter spp. are a leading cause of zoonotic enteric illness in most developed countries (Friedman et al., 2000[5]). Human cases are usually caused by C. jejuni, and to a lesser extent, by Campylobacter coli. Information on the burden of human campylobacteriosis in developing countries is more limited (Oberhelman & Taylor, 2000[6]). Nevertheless, it is reported that asymptomatic infection with C. jejuni and C. coli is frequent in adults. In children, under the age of two, C. jejuni, C. coli and other Campylobacter spp. are all associated with enteric disease.

Campylobacter spp. may be transferred to humans by direct contact with contaminated animals or animal carcasses or indirectly through the ingestion of contaminated food or water. The principal reservoirs of thermophilic Campylobacter spp. are the alimentary tracts of wild and domesticated mammals and birds. Campylobacter spp. are commonly found in poultry, cattle, pigs, sheep, wild animals and birds, and in dogs and cats. Foodstuffs, including, poultry, beef, pork, other meat products, raw milk and milk products, and, less frequently, fish and fish products, mussels and fresh vegetables can also be contaminated (Jacobs-Reitsma, 2000[7]). Findings of analytical epidemiological studies are conflicting. Some have identified handling raw poultry and eating poultry products as important risk factors for sporadic campylobacteriosis (Friedman, et al., 2000[5]), however others have found that contact in the home with such products is protective (Adak et al., 1995[8]).

Information for the hazard identification section was compiled from published literature and from unpublished data submitted to FAO and WHO by public health agencies and other interested parties. Hazard characterization

Hazard characterization provides a description of the public health outcomes following infection, including sequelae, pathogen characteristics influencing the organism's ability to elicit infection and illness, host characteristics that influence the acquisition of infection, and food-related factors that may affect the survival of C. jejuni in the human gastrointestinal tract. A dose-response model was derived that mathematically describes the relationship between the numbers of organisms that might be present in a food and consumed (the dose), and the human health outcome (the response). In order to achieve this, human feeding trial data (Black et al., 1988[9]) for two strains of C jejuni were pooled and used to derive estimates for the probability of infection (colonization of the gastrointestinal track without overt symptoms) as well as the probability of illness once infected. Campylobacteriosis predominantly occurs as sporadic cases (Friedman, et al., 2000[10]), and hence dose-response data from outbreak investigations are essentially non-existent.

The probability of infection upon ingestion of a dose of C. jejuni was estimated with the caveat that the data are from a feeding study involving healthy volunteers, and using a milk matrix and a limited number of campylobacter strains. Whether the probability of infection and/or illness are different for immune individuals or those individuals with an increased susceptibility to illness (e.g. immunosuppressed, very young, etc.) compared to the volunteers could not be determined from the feeding trial data. The probability of illness following infection was also estimated based upon these investigations, and assumed to be dose-independent. Again, the impact of other factors, such as susceptibility, on the probability of illness cannot be quantified due to a lack of adequate epidemiological data and resolution to this level. The progression of the illness to more serious outcomes and the development of some sequelae can be crudely estimated from the approximate proportions reported in the literature, but these were not included in the present work. For the purposes of this model it was assumed that C. coli has the same properties as C. jejuni. Exposure assessment

The exposure model describes the stages Rearing and Transport, Slaughter and Processing, and Preparation and Consumption (Figure 5.1). This modular approach estimates the prevalence and concentration of thermophilic Campylobacter spp., and the changes in these associated with each stage of processing, and refrigerated and frozen storage and consumer handling of the product.

Routes contributing to initial introduction of Campylobacter spp. into a poultry flock[11] on the farm have been identified in epidemiological studies. However, these remain poorly understood and the phenomenon may be multi-factorial, and hence, colonization was modelled based on an unspecified route of introduction. However, an epidemiology module has been created as a supplement to the model, which allows evaluation of interventions aimed at changing the frequency with which risk factors occur. As such risk factors are usually interdependent and may be country specific, incorporation of this module into the current risk model was not appropriate: however, it does illustrate how such information may be used in a specific situation.

The effects of cooling and freezing, and adding chlorine during water chilling, are evaluated in the model. Effects of other processing treatments, e.g. lactic acid and irradiation, on reduction of Campylobacter spp. contamination on poultry carcasses were not explicitly evaluated as the quantitative data are lacking: however, if the level of reduction as a consequence of any type of processing modification, can be quantified for any treatment, then the impact on risk can be readily evaluated within the risk model.

The home preparation module considered two routes of ingestion of viable organisms: via consumption of contaminated, undercooked chicken meat, and via cross-contamination, from contaminated raw poultry onto another food that is eaten without further cooking, or directly from the hands (Figure 5.2). As a result of recommendations from the previous expert consultation[12] the "protected areas" cooking approach and the drip-fluid model approach for cross-contamination were selected. The "protected areas" approach to modelling the cooking step considers that campylobacter cells may be located in parts of the carcass that reach cooking temperature more slowly than other locations. The drip-fluid model for cross-contamination relates to the spread of campylobacter cells via drip-fluid from raw carcasses.

FIGURE 5.2: Schematic representation of the home preparation module. Risk characterization

The risk characterization step integrates the information collected during the hazard identification, hazard characterization, and exposure assessment steps to arrive at estimates of adverse events that may arise due to consumption of chicken (Figure 5.1). This step links the probability and magnitude of exposure to campylobacter associated with consumption of chicken to adverse outcomes that might occur. The resulting risk is expressed as individual risk or the risk per serving of chicken. Although this model does not address risk to a specific population, data on amounts of chicken consumed can be incorporated into the model to arrive at estimates of the population-based risk.

The current model is unable to provide a central estimate of risk due to virtually unbounded uncertainty[13] on two key components of the model, namely the impact of undercooking and the impact of cross-contamination. Since these processes are the ultimate determinant of the final exposure of the consumer, the unbounded and unresolvable nature of the uncertainty undermines the establishment of a central estimate of consumer risk. In addition, the model has not yet been applied to explore the upper and lower bound estimates of risk that are suggested by the uncertainty. However, the model still provides a useful means of studying potential exposure pathways and how these contribute to the risk of illness posed by campylobacter associated with broiler chickens.

The risk characterization involves the following elements:

1) A baseline model

A baseline model was explored in detail, to clarify the input-output relations between the different modules of the model and also to explore the credibility of the model. The baseline model was defined as the processing of fresh carcasses from both positive and negative flocks (with an overall flock prevalence of 80%), which are air chilled at the end of slaughter.

The model indicated that the external campylobacter load per chicken increased during transport and evisceration, and decreased at the other processing steps studied, with an overall reduction of the mean load from farm to fork of about 4 to 5 logs (Figure 5.3). The prevalence of campylobacter-contaminated chickens from positive flocks appears to drop from 100% of live birds to 20% of chicken meat servings (Figure 5.4). For negative flocks, prevalence increases during transport, defeathering and evisceration, indicating the effect of cross-contamination during processing. Prevalence later drops to a value of about 3% of servings at the moment of consumption.

The correlation between the input and output of the models of the different processing steps has been graphed to illustrate the variability in load per chicken along the process. These plots indicate that the load on a chicken at the stages before evisceration appears to be a bad predictor for the final load, and thus for the risk per serving of that particular chicken carcass.

2) Scenario analysis

In a scenario analysis, the effects of alterations to the baseline are studied by changing one or two of the model parameters. By doing so the impact of uncertainty in parameter estimates can be explored, and the potential of risk mitigation strategies can be evaluated.

Eight alternative scenarios were explored, to illustrate the ability of the model to investigate the effect of changing specific model inputs. Each individual scenario involved a specific change in one parameter, as follows:

Mitigation related scenarios

1. Between flock[14] prevalence (80% prevalence reduced to 50%)
2. Within flock prevalence (100% prevalence reduced to 10%)
3. Scalding (hard scald (56-58°C for 2-2.5 minutes)and soft scald (50-52 °C for up to 3.5 minutes))

Alternate model assumption scenarios

4. Shorter freezing storage time range (1 day to 6 weeks storage time compared to 1 day to 1 week storage time)

5. Undercooking (5°C lower temperature in coolest spot in the chicken during cooking)

6. Defeathering (an increase in the magnitude of cross-contamination)

7. Contamination during water chilling without chlorine (a decrease of the contamination added)

8. Contamination during water chilling with chlorine (decrease of the contamination added)

The largest effects were observed with lower undercooking temperature, which led to an increase in risk and lower within flock prevalence, which led to a decrease in risk.

FIGURE 5.3: Numbers of campylobacter cells per carcass during processing of fresh air-chilled carcasses, from both positive and negative flocks. (Negative flocks get contaminated during transport). Both the mean of the logs and the log of the means are given. (The differences between these is as a result of the skewness[15] of the distribution of values and the fact that 'zero'- values cannot be incorporated in calculations of the mean of logs (which is therefore only about the positive carcasses)).

FIGURE 5.4: The prevalence of campylobacter on fresh air-chilled broiler chicken carcasses coming from flocks that were positive and negative for campylobacter at the farm level.

To further detail the model analysis, and to determine the effect of introducing different mitigations, five series of simulations were run. Using the baseline model settings one of following parameters was changed in each series of simulations:

A linear relationship between flock prevalence and probability of illness was found. Thus a two-fold reduction in flock prevalence would result in a corresponding two-fold reduction in the probability of illness. This effect is mainly caused by a reduction in the number of campylobacter-positive meals. Both external contamination and colonization need to be reduced concurrently to achieve a substantial impact on risk. This is due to the potential for large numbers of campylobacter cells contaminating the carcass as a result of damage to the viscera at evisceration, thus undermining any benefits achieved in reducing the external numbers at an earlier processing step. Use of the model has identified two key ways of achieving this reduction: 1) reducing colonization early enough to impact external contamination and 2) intervening post-evisceration to reduce carcass contamination.

5.1.4 Key findings

1. There is a lack of systematic and fundamental investigation into the key processes throughout the production-to-consumption continuum that may lead to human infection as a result of chicken consumption. This was evidenced by the extensive knowledge acquired and data gaps identified during this risk assessment.

2. Quantifying and characterizing uncertainty, although often recommended, needs to be recognized as a task that can be unfeasible, and relatively unrewarding, in situations where the model contains:

a. many uncertain parameters (lack of data and information to inform the parameters of the model),

b. a large amount of uncertainty (lack of data and information to inform the mathematical description of how the system works, including causal relationships and dependencies), or

c. a risk assessment simulation model that is complex (constraints in computing ability in order to perform the quantification).

In the case of this risk assessment, all three of these properties apply. Although there were numerous quantifiable uncertainties, it was believed that model uncertainties (point b, above) would dominate the total uncertainty. The extent of the model uncertainties was such that the magnitude of the quantifiable uncertainties would be rendered irrelevant.

3. It was difficult to model cross-contamination in the home as a result of the lack of a clear understanding of the pathways and lack of data quantifying the magnitude and frequency of cross-contamination events. Further improvement of this module and validation may be extremely difficult given the complexity of cross-contamination, the many possible pathways by which it can occur, and the variability in the behaviour of individuals in the kitchen.

4. Based on thermal inactivation calculations, it was difficult to reconcile the assumed importance of undercooking as a cause of human exposure to campylobacter, if the contamination of broiler carcasses with campylobacter is on the external surface of the carcass (or very close to the surface). Resolution of this inconsistency requires the allocation of some amount of contamination to sub-surface sites within the carcass where the temperature increases much more slowly. While it is possible to demonstrate that campylobacter will, on occasion, be found in such places, it is very difficult to quantify the frequency and extent of this particular mode of contamination.

5. Overall campylobacter concentration on chicken carcasses decreased through processing, with temporary increases occurring during transport and evisceration.

6. The prevalence of campylobacter-positive carcasses from negative flocks increased up to and including evisceration and decreased at later stages. This decrease after evisceration was also found for positive flocks, depending upon the method of chilling.

7. The campylobacter load on a chicken at the stages before evisceration was identified as a bad predictor for the final load, and thus for the risk per serving of that particular chicken.

8. Assuming that cooking performance is independent of the chicken being fresh or frozen, frozen chicken posed a lower risk via consumption than fresh chicken.

9. The washing-off effect associated with water chilling translated to water-chilled chickens posing a lower risk than air-chilled chickens. However, there was uncertainty associated with the degree of cross-contamination that occurs in the chill tank during water chilling that would have an impact on this comparison and may be affected by the addition of chlorine to the chill water.

10. Undercooking was estimated to have a higher risk than cross-contamination using one set of assumptions. The cooking and cross-contamination modules are based on plausible theoretical constructs, but knowledge and data related to these two pathways are essentially unavailable. Since the set of assumptions on which this comparison relied was only one, of many, plausible sets, analysis of this component of the model remains inconclusive.

11. Unlike many other mitigation scenarios, there was very little uncertainty that reduction of the between-flock prevalence of campylobacter would reduce any associated public health risk. A linear relationship was found to exist between flock prevalence and probability of illness, i.e. a two-fold reduction in flock prevalence would result in a corresponding two-fold reduction in the probability of illness.

12. In order to meaningfully reduce the bacterial load on processed carcasses, interventions would be required to address the bacterial load both internally and externally, since efforts directed at only one of these contamination reservoirs can be readily undermined by high levels of contamination from the other.

5.1.5 Risk assessment and developing countries

The current risk assessment document also addressed the issue of whether it is possible for developing countries to apply the concepts and use the components from this model to conduct their own quantitative risk assessment. The relative complexity of the current model was recognized. It is relevant to poultry produced and processed under conditions similar to those described in the risk assessment and so, in particular, may be applicable to the large-scale production and processing facilities in developing countries. However, many of the exposure elements in developing countries - the consumption patterns, slaughter processes and farming practices - may be quite different from those described here, thus limiting the applicability of the risk assessment. Furthermore, there are few, if any, data on exposure routes, risk factors and human illness associated with campylobacter in developing countries. Thus, the possibility of performing a national quantitative microbial risk assessment may require a capacity that does not currently exist in many developing countries. There are steps that developing countries can take to aid future risk assessment efforts. A knowledge of risk management activities, which initiate and facilitate the risk assessment process, are important. The "Guidelines for incorporating quantitative risk assessment in the development of microbiological food hygiene standards, guidelines and related texts"[16] currently being elaborated by FAO and WHO includes guidance on preliminary risk management activities which are critical in structuring the risk assessment process. Data collection, one of the most important related activities, received particular attention, and focus was given to the main tasks that need to be undertaken.

5.1.6 Limitations and caveats

The expert consultation identified features of the assessment that have an impact on the acceptability of the model and the appropriateness of using this model. The model was developed so as not to be representative of any specific country or region. Yet many of the model inputs were based on data and processing practices in one country. Prior to using the model to predict risk for a specific country, data, that is representative of that country, should be used to determine model inputs.

A hypothetical baseline scenario was considered in order to evaluate the relative merit of control strategies for campylobacter in broiler chickens. This scenario consists of a compromise of input assumptions derived from a range of countries. The findings from the baseline scenario should not be used to draw inferences about a particular nation or region. To make specific inferences it would be necessary to collect inputs that were directly relevant to the particular population of interest.

Although the uncertainty associated with several parameters in the consumption portion of the risk assessment was accounted for, a full analysis of statistical and model uncertainty was not performed. This is explained in section 5.1.4. (under 2).

The data available for generation of the dose-response curve was limited to one feeding trial study (see section An alteration to our current understanding of the dose-response relationship, which may occur if for example additional dose-response information became available, would result in changes in the risk estimates generated by the model.

5.1.7 Gaps in the data

In the course of undertaking this risk assessment, it was found that appropriate data was not always available and this limited the extent to which the risk assessment could be completed. The main data gaps that were identified are outlined below.

Exposure assessment: On-farm

Exposure assessment: Processing

Exposure assessment: Post-processing and consumer handling

Hazard Characterization

5.2 Review of the Risk Assessment

The expert consultation reviewed the document entitled "Preliminary Report - A Draft Risk Assessment of Campylobacter spp. in Broiler Chickens" (MRA02/01) and the presentation of additional data by the drafting group. It acknowledged the extensive work undertaken by the risk assessment drafting group and reviewed the components of the risk assessment document, the outcome of which is summarized below.

5.2.1 Introduction

The expert consultation highlighted the importance of including in the introduction of the final risk assessment document a succinct, clear description of the history of this exercise: by whom it was initiated; what reports have been produced, and when. The objectives of the risk assessment should be more clearly stated, with reference to who suggested them. Objectives which have been specifically excluded should also be listed. It would be useful to state whether each objective has been achieved and if not, why not. This would facilitate a better understanding of the work and why it was developed in such a manner. Descriptions of methods and approaches should not appear in this section.

A concluding paragraph suggesting the steps to be taken following the successful conclusion of this initiative would be beneficial to the end-users, while also stressing that no risk assessment model is complete as long as data gaps exist.

5.2.2 Hazard identification

The final risk assessment document will require an up-to-date review of hazard identification associated with Campylobacter spp. and campylobacteriosis in humans and animals.

5.2.3 Exposure assessment: Campylobacter in poultry on the farm and during transportation:

The main features of this module are:

This part of the model assumes that:

Data deficiencies and recommendations for model improvements

It is evident that the reduction or elimination of campylobacter colonization in the flock is extremely important. At the farm level there are limited strategies to achieve this aim. Approaches include preventing flock exposure by biosecurity or reducing bird susceptibility to colonization by measures such as vaccination or competitive exclusion treatment (Newell & Wagenaar, 2000[17]). The latter approaches are not yet available commercially and, therefore, biosecurity is the only strategy currently feasible. A module to assess the relative importance of sources of colonization would be extremely useful to risk managers, and such a module has been initiated. However, it was considered by the risk assessment drafting group that there were at this time insufficient data on flock infection sources for the use of such a module.

The part of the model dealing with the effect of catchers contaminating the exterior of birds could, with some modification, be adapted to model the effects of thinning (the early removal of a proportion of the birds) which is considered a major source of broiler colonization.

Using data on between-flock and within-flock prevalence of campylobacter the probability of any random bird being campylobacter-positive can be estimated. The model also demonstrates that the probability of colonization is dependant on age which is consistent with available data (Newell and Wagenaar, 2000[17]). Although the model can indicate the effect of various generic sources on transmission it cannot, at this time, allow an assessment of the sources of exposure to provide targeted strategies for intervention. Processing

The main features of this module are:

This part of the model assumes that:

Data deficiencies and recommendations for model improvements

The poultry production industry has substantially improved hygiene control over the last 30 years. Many of the changes may have effects on the data entered into the model, for example the introduction of multistage scalding and newer evisceration machinery which separates the viscera from the carcass. If there are data or evidence that such changes have a significant effect on campylobacter contamination of carcasses then appropriate changes to the model should be considered.

Overall, the spread of contamination from the gut contents of positive birds will have the greatest effect on the level of contamination on external bird surfaces. However, as the proportion of negative flocks increases, the importance of cross-contamination becomes more apparent. Data is now being collected for the level of contamination on carcasses from campylobacter-negative flocks. This data should be available in the near future, and the expert consultation recommended that at that time it should, if possible, be incorporated into the model.

The model should take account of the published and unpublished data showing that organisms attached to the carcass surface are resistant to environmental effects. (Notermans and Kemplemaker, 1975[20]; G. Mead, personal communication, 2002).

Only freezing and chilled storage were considered in the post-processing part of this module. Recent anecdotal data indicates that modified atmosphere packaging has an impact on levels of campylobacter contamination on poultry products. The expert consultation recommended that when this data comes into the public domain it should, if possible, be incorporated into this module.

There is increasing evidence for variation in the survival of campylobacter strains during processing (Newell et al., 2001[21]). This may have a considerable effect on the model especially if the ability of Campylobacter spp. to survive is associated with strain virulence. At this time there are no simple methods for assessing the ability to survive but models for this property are available and data is currently being accumulated. Once this data becomes available the expert consultation recommended that it should, if possible, be incorporated into this module. Consumer handling and cooking

The main features of this part of the model are:

This part of the model assumes that:

Data deficiencies and recommendations for model improvements

More information is required on consumer practices in domestic kitchens. Information is needed on routes and modes of transmission of campylobacter within the kitchen. Factors affecting campylobacter survival in the kitchen environment are also required.

5.2.4 Hazard characterization

Due to the lack of new data on the dose-response relationship for campylobacter, no further progress can been made in this area. Similarly there is currently a paucity of data on the proportion of campylobacter strains in poultry which are virulent in humans and to which humans are susceptible.

5.2.5 Risk characterization

As highlighted in section there is a lot of uncertainty associated with the current model, primarily due to the lack of information on the impact of undercooking and cross-contamination on exposure of the consumer to campylobacter. The expert consultation could not foresee that this uncertainty would be significantly reduced in the near future. However, despite this situation, the expert consultation noted that the model could be applied to explore the sensitivity of the risk estimates to a broad range of plausible alternate models and parameters. In addition, as much contextual information as possible on the uncertainty and its implication should be provided for risk managers and also researchers in this area so that consideration can be given as to how this uncertainty can be reduced.

The model remains very useful to study the biological and systematic plausibility of alternate hypotheses regarding these exposure pathways and will contribute to the understanding of the risk posed through these two pathways.

The expert consultation noted that for certain combinations of model parameters a 10-fold reduction in the probability of infection from a single serving had a dramatic effect on the probability of illness (about 4-fold). However, only preliminary results were available as work was ongoing to refine this section. In doing so the expert consultation recommended that the effect combined mitigations (e.g. vaccination and freezing) also be evaluated using the model.

5.2.6 Risk assessment and developing countries

It was noted that the problem of campylobacteriosis in developing countries, at a national public health level, may be considerably different from that in developed countries (Oberhelman and Taylor, 2000[22]). Epidemiological features of campylobacteriosis are distinct and suggest more frequent exposures from various sources. There is substantial and increasing evidence that immunity as a consequence of repeated exposure plays an important role in protection against campylobacteriosis (Cawthraw et al., 2000[23]) and this may be particularly relevant in developing countries (Newell & Nachamkin, 1992[24]). It was recommended that such countries take this factor into account when applying the model.

One of the most important issues for developing countries is whether the application of the risk assessment model is appropriate at all. The model may be usefully adapted for the exporting poultry industry in such countries, as it is anticipated that such commercial operations will be similar to those in developed countries. However, for domestic public health purposes, the current risk assessment model would need considerable adaptation. In particular, chicken processing practices may be less standardized and more variable. Moreover, food habits are likely to vary and the immune status of the population is expected to be different.

5.2.7 Data deficiencies

There are numerous data gaps which have precluded the development of a complete risk model. Therefore, the deliberate omission of uncertainty analysis in the model was accepted by the expert consultation.

It was recognized that, for further development of the model, new data are clearly needed and are also required to facilitate selection of appropriate interventions measures by risk managers.

The expert consultation identified the following research priorities, however, it is critical to note that research priorities will vary depending on the specific risk management question the risk assessment is being used to address.

A. Exposure assessment

B. Hazard characterization

5.3 Utility and Applicability

The expert consultation recognized this risk assessment as a resource that can be used by many parties including national authorities. The current document provides a framework for undertaking risk assessment of thermophilic Campylobacter spp. in broiler chickens, a modelling approach that can be adapted to various situations and a unique source of data and other relevant information. While it does not overcome the need to establish a risk assessment team at the national level it will significantly reduce the workload of such a team and the time they require to carry out a risk assessment. This exercise has also led to the identification of the types of data that are required for risk assessment. While, it was noted that the collection of such data will depend on the purpose for which the risk assessment is being undertaken, the risk assessment nonetheless highlights a number of areas where data generation activities may need to be focussed.

Furthermore, the model in its current form can be used by risk managers to help them make decisions on the suitability of specific interventions. Given information on the efficacy of an intervention, the relative reduction in the number of possible cases of illness can be assessed. More specific issues in relation to the utility of this work are elaborated on below.

Applicability of the model to different production systems

The model described in the risk assessment has been developed to estimate the risk of thermophilic campylobacter from broiler chickens produced under a specified production system. The model is an example of how a risk assessment could be undertaken and details mathematical models that might be used to describe production practices. In order for the model to be used in different countries it must be modified to reflect prevailing practices.

Utility of the model to risk assessors

The model contains all the elements necessary to enable risk modellers to perform risk assessments for their own production systems. The modular approach used enables modellers to utilize various components of the model individually or collectively. When finally presented the model should be structured in a clear and concise way. This is important if the model is to be used as a tool to aid modellers in conducting risk assessments.

Utility of the model to Risk Managers

Communication is a critical element in ensuring the risk assessment model is of use to risk managers. The model should not be used by risk managers without the aid and advice of competent risk assessors, who can explain the assumptions and uncertainties associated with the model. For example in the current model cooking and cross-contamination are not modelled on ‘real’ data, because such data are not yet available. The expert consultation noted the limitations placed on the utility of the model by the absence of evidence and lack of consensus among experts on the relative importance of cross-contamination.

5.4 Response to the specific risk management questions posed by the Codex Committee on Food Hygiene

As noted by the previous expert consultation on Campylobacter spp. in broiler chickens[25] the risk management questions posed by the CCFH were not tailored to the particular problem of campylobacter in chicken.

At a meeting of a CCFH drafting group[26], established by the committee to develop a discussion paper on risk management strategies for campylobacter in poultry, it was considered that the provision of guidance to the risk managers on the relative efficacy of mitigation strategies would be a useful outcome of the risk assessment. Given this, it was decided that interventions at various points in the overall process would be investigated rather than the investigation of any specific mitigation strategy.

Five scenarios were selected, one dealing with the effect of changing the flock prevalence and four others looking at the effect of reducing campylobacter load, either on the exterior of the chickens at slaughter or in the chickens gut before slaughter. The outcome of these scenarios are presented in the risk characterization and key findings sections ( & 5.1.5).

Applying the campylobacter risk assessment to particular regions or areas will require the collection and input of data specific for local conditions. Similarly the risk assessment model may need adaptation. The risk assessment model should be used by a risk analysis team including risk assessors. The needs of risk managers must be considered as must the limitations imposed by economic, political, consumer and stakeholder priorities.

5.5 Conclusions and Recommendations

The risk assessment model utilizes a modular approach that is applicable to the entire poultry supply chain. It is flexible to use and capable of dealing with a range of issues relating to campylobacter contamination and its control in poultry from production-to-consumption. The exercise described in the report has covered both the conceptual development of the model and the evaluation of data needed to demonstrate its value. For practical application, however, the model would need to be modified, adapted or even redeveloped to suit the differing circumstances of individual users. The model takes no account of uncertainty because data are lacking on this aspect. In relation to developing countries, the model is particularly relevant to conditions of intensive production and processing that occur where poultry meat is exported. While it could also be adapted to the free range "village chicken" that is a feature of many developing countries, the expert consultation was not aware of any evidence on the risk to public health from this type of bird.

The expert consultation recognized the uncertainties surrounding the relative importance of undercooking and cross-contamination in the kitchen but, from epidemiological evidence, were of the opinion that cross-contamination was the more important factor.

The expert consultation made a number of recommendations aimed at improving the transparency and utility of the risk assessment document:

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[8] Adak, G. K., Cowden, J. M., Nicholas, S. & Evans, H. S. 1995. The Public Health Laboratory Service national case-control study of primary indigenous sporadic cases of campylobacter infection. Epidemiology and Infection 115, 15-22.
[9] Black, R. E., Levine, M. M., Clements, M. L., Hughes, T. P. & Blaser, M. J. 1988. Experimental Campylobacter jejuni infection in humans. Journal of Infectious Diseases 157, 472-9.
[10] Friedman, C., Neimann, J., Wegener, H. & Tauxe, R. 2000. Epidemiology of Campylobacter jejuni infections in the United States and other industrialized nations. In Campylobacter 2nd Edition, pp. 121-138. Edited by I. Nachamkin & M. J. Blaser. Washington DC: ASM Press.
[11] A flock is a group of hens of similar age that are managed and housed together.
[12] WHO. 2001. Report of the Joint FAO/WHO Expert Consultation on Risk Assessment of Microbiological Hazards in Foods; Hazard identification, exposure assessment and hazard characterization of Campylobacter spp. in broiler chickens and Vibrio spp. in seafood. WHO Headquarters, Geneva, Switzerland 23 - 27 July 2001. WHO 2001.
[13] As the upper and lower boundaries of the values describing the impact of undercooking and cross-contamination are unknown the distribution of possible values is potentially infinite and therefore unbounded.
[14] Between flock refers to different groups of hens (i.e. different flocks).
[15] Skewness is a statistical term that refers to the lobsideness of a distribution.
[16] The process of elaborating FAO/WHO "Guidelines for incorporating quantitative risk assessment in the development of microbiological food hygiene standards, guidelines and related texts" began at a consultation convened in Kiel, Germany on 18 - 22 March 2002. The draft guidelines are currently being finalized and will be available on the FAO and WHO webpages at the end of 2002.
[17] Newell, D. G. & Wagenaar, J. A. 2000. Poultry infections and their control at the farm level. In Campylobacter, 2nd Ed., pp. 497-509. Edited by I. Nachamkin & M. J. Blaser. Washington DC: ASM Press.
[18] Jacobs-Reitsma, W. 2000. Campylobacter in the food supply. In Campylobacter 2nd Ed., pp. 467-481. Edited by I. Nachamkin & M. J. Blaser. Washington DC: ASM Press.
[19] Mead G.C. 1989. Hygiene problems and control of process contamination. In: Processing of poultry (ed Mead G.C.) Chapman Hall, London.pp 183-220.
[20] Notermans S. and Kamplemaker E.H. 1975. Heat destruction of some bacterial strains attached to broiler skin. British Poultry Science, 16: 351-361
[21] Newell, D. G., Shreeve, J. E., Toszeghy, M., Domingue, G., Bull, S., Humphrey, T. & Mead, G. 2001. Changes in the carriage of campylobacter strains by poultry carcasses during processing in abattoirs. Applied and Environmental Microbiology. 67, 2636-40.
[22] Oberhelman, R. & Taylor, D. 2000. Campylobacter infections in developing countries. In Campylobacter 2nd Edition, pp. 139-154. Edited by I. Nachamkin & M. Blaser. Washington DC: ASM Press.
[23] Cawthraw, S. A., Lind, L., Kaijser, B. & Newell, D. G. 2000. Antibodies, directed towards Campylobacter jejuni antigens, in sera from poultry abattoir workers. Clinical and Experimental Immunology 122, 55-60.
[24] Newell, D. & Nachamkin, I. 1992. Immune responses directed against Campylobacter jejuni. In Campylobacter jejuni: Current staus and future trends, pp. 201-206. Edited by I. Nachamkin, M. Blaser & L. Tompkins. Washington DC: ASM Press.
[25] WHO. 2001. Joint FAO/WHO Expert Consultation on Risk Assessment of Microbiological Hazards in Foods; Hazard identification, exposure assessment and hazard characterization of Campylobacter spp. in broiler chickens and Vibrio spp. in seafood, WHO Headquarters, Geneva, Switzerland 213 - 27 July 2001. WHO 2001.
[26] Report of the thirty fourth session of the Codex Committee on Food Hygiene, Bangkok, Thailand, 8 - 13 October 2001 ALINORM 03/13 para. 77.

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