Quantitative risk assessment-epidemic curve prediction model for leafy green outbreak investigation

The objective of this study was to leverage quantitative risk assessment to investigate possible root cause(s) of foodborne illness outbreaks related to Shiga toxin-producing Escherichia coli O157:H7 (STEC O157) infections in leafy greens in the United States. To this end, we developed the FDA leafy green quantitative risk assessment epidemic curve prediction model (FDA-LG QRA-EC) that simulated the lettuce supply chain. The model was used to predict the number of reported illnesses and the epidemic curve associated with lettuce contaminated with STEC O157 for a wide range of scenarios representing various contamination conditions and facility processing/sanitation practices. Model predictions were generated for fresh-cut and whole lettuce, quantifying the differing impacts of facility processing and home preparation on predicted illnesses. Our model revealed that the timespan (i.e., number of days with at least one reported illness) and the peak (i.e., day with the most predicted number of reported illnesses) of the epidemic curve of a STEC O157-lettuce outbreak were not strongly influenced by facility processing/sanitation practices and were indications of contamination pattern among incoming lettuce batches received by the facility or distribution center. Through comparisons with observed number of illnesses from recent STEC O157-lettuce outbreaks, the model identified contamination conditions on incoming lettuce heads that could result in an outbreak of similar size, which can be used to narrow down potential root cause hypotheses.     

Salmonella Prevalence Alone Is Not a Good Indicator of Poultry Food Safety

Salmonella is a leading cause of foodborne illness (i.e., salmonellosis) outbreaks, which on occasion are attributed to ground turkey. The poultry industry uses Salmonella prevalence as an indicator of food safety. However, Salmonella prevalence is only one of several factors that determine risk of salmonellosis. Consequently, a model for predicting risk of salmonellosis from individual lots of ground turkey as a function of Salmonella prevalence and other risk factors was developed. Data for Salmonella contamination (prevalence, number, and serotype) of ground turkey were collected at meal preparation. Scenario analysis was used to evaluate effects of model variables on risk of salmonellosis. Epidemiological data were used to simulate Salmonella serotype virulence in a dose‐response model that was based on human outbreak and feeding trial data. Salmonella prevalence was 26% (n = 100) per 25 g of ground turkey, whereas Salmonella number ranged from 0 to 1.603 with a median of 0.185 log per 25 g. Risk of salmonellosis (total arbitrary units (AU) per lot) was affected (p ≤ 0.05) by Salmonella prevalence, number, and virulence, by incidence and extent of undercooking, and by food consumption behavior and host resistance but was not (p > 0.05) affected by serving size, serving size distribution, or total bacterial load of ground turkey when all other risk factors were held constant. When other risk factors were not held constant, Salmonella prevalence was not correlated (r = ?0.39; p = 0.21) with risk of salmonellosis. Thus, Salmonella prevalence alone was not a good indicator of poultry food safety because other factors were found to alter risk of salmonellosis. In conclusion, a more holistic approach to poultry food safety, such as the process risk model developed in the present study, is needed to better protect public health from foodborne pathogens like Salmonella.     

A Stochastic Model to Assess the Effect of Meat Inspection Practices on the Contamination of the Pig Carcasses

The objective of meat inspection is to promote animal and public health by preventing, detecting, and controlling hazards originating from animals. With the improvements of sanitary level in pig herds, the hazards profile has shifted and the inspection procedures no longer target major foodborne pathogens (i.e., not risk based). Additionally, carcass manipulations performed when searching for macroscopic lesions can lead to cross‐contamination. We therefore developed a stochastic model to quantitatively describe cross‐contamination when consecutive carcasses are submitted to classic inspection procedures. The microbial hazard used to illustrate the model was Salmonella, the data set was obtained from Brazilian slaughterhouses, and some simplifying assumptions were made. The model predicted that due to cross‐contamination during inspection, the prevalence of contaminated carcass surfaces increased from 1.2% to 95.7%, whereas the mean contamination on contaminated surfaces decreased from 1 logCFU/cm² to ?0.87 logCFU/cm², and the standard deviations decreased from 0.65 to 0.19. These results are explained by the fact that, due to carcass manipulations with hands, knives, and hooks, including the cutting of contaminated lymph nodes, Salmonella is transferred to previously uncontaminated carcasses, but in small quantities. These small quantities can easily go undetected during sampling. Sensitivity analyses gave insight into the model performance and showed that the touching and cutting of lymph nodes during inspection can be an important source of carcass contamination. The model can serve as a tool to support discussions on the modernization of pig carcass inspection.     

A Multifactorial Risk Prioritization Framework for Foodborne Pathogens

We develop a prioritization framework for foodborne risks that considers public health impact as well as three other factors (market impact, consumer risk acceptance and perception, and social sensitivity). Canadian case studies are presented for six pathogen‐food combinations: Campylobacter spp. in chicken; Salmonella spp. in chicken and spinach; Escherichia coli O157 in spinach and beef; and Listeria monocytogenes in ready‐to‐eat meats. Public health impact is measured by disability‐adjusted life years and the cost of illness. Market impact is quantified by the economic importance of the domestic market. Likert‐type scales are used to capture consumer perception and acceptance of risk and social sensitivity to impacts on vulnerable consumer groups and industries. Risk ranking is facilitated through the development of a knowledge database presented in the format of info cards and the use of multicriteria decision analysis (MCDA) to aggregate the four factors. Three scenarios representing different stakeholders illustrate the use of MCDA to arrive at rankings of pathogen‐food combinations that reflect different criteria weights. The framework provides a flexible instrument to support policymakers in complex risk prioritization decision making when different stakeholder groups are involved and when multiple pathogen‐food combinations are compared.     

Diminishing Willingness to Pay per Quality‐Adjusted Life Year: Valuing Acute Foodborne Illness

We design and conduct a stated‐preference survey to estimate willingness to pay (WTP) to reduce foodborne risk of acute illness and to test whether WTP is proportional to the corresponding gain in expected quality‐adjusted life years (QALYs). If QALYs measure utility for health, then economic theory requires WTP to be nearly proportional to changes in both health quality and duration of illness and WTP could be estimated by multiplying the expected change in QALYs by an appropriate monetary value. WTP is elicited using double‐bounded, dichotomous‐choice questions in which respondents (randomly selected from the U.S. general adult population, n = 2,858) decide whether to purchase a more expensive food to reduce the risk of foodborne illness. Health risks vary by baseline probability of illness, reduction in probability, duration and severity of illness, and conditional probability of mortality. The expected gain in QALYs is calculated using respondent‐assessed decrements in health‐related quality of life if ill combined with the duration of illness and reduction in probability specified in the survey. We find sharply diminishing marginal WTP for severity and duration of illness prevented. Our results suggest that individuals do not have a constant rate of WTP per QALY, which implies that WTP cannot be accurately estimated by multiplying the change in QALYs by an appropriate monetary value.     

Risk of Illness with Salmonella due to Consumption of Raw Unwashed Vegetables Irrigated with Water from the Bogotá River

The Bogotá River receives untreated wastewater from the city of Bogotá and many other towns. Downstream from Bogotá, water from the river is used for irrigation of crops. Concentrations of indicator organisms in the river are high, which is consistent with fecal contamination. To investigate the probability of illness due to exposure to enteric pathogens from the river, specifically Salmonella, we took water samples from the Bogotá River at six sampling locations in an area where untreated water from the river is used for irrigation of lettuce, broccoli, and cabbage. Salmonella concentrations were quantified by direct isolation and qPCR. Concentrations differed, depending on the quantification technique used, ranging between 10^7.7 and 10^9.9 number of copies of gene invA per L and 10^5.3 and 10^8.4 CFU/L, for qPCR and direct isolation, respectively. A quantitative microbial risk assessment model that estimates the daily risk of illness with Salmonella resulting from consuming raw unwashed vegetables irrigated with water from the Bogotá River was constructed using the Salmonella concentration data. The daily probability of illness from eating raw unwashed vegetables ranged between 0.62 and 0.85, 0.64 and 0.86, and 0.64 and 0.85 based on concentrations estimated by qPCR (0.47–0.85, 0.47–0.86, and 0.41–0.85 based on concentrations estimated by direct isolation) for lettuce, cabbage, and broccoli, respectively, which are all above the commonly propounded benchmark of 10^?4 per year. Results obtained in this study highlight the necessity for appropriate wastewater treatment in the region, and emphasize the importance of postharvest practices, such as washing, disinfecting, and cooking.     

An Agent‐Based Model for Pathogen Persistence and Cross‐Contamination Dynamics in a Food Facility

We used an agent‐based modeling (ABM) framework and developed a mathematical model to explain the complex dynamics of microbial persistence and spread within a food facility and to aid risk managers in identifying effective mitigation options. The model explicitly considered personal hygiene practices by food handlers as well as their activities and simulated a spatially explicit dynamic system representing complex interaction patterns among food handlers, facility environment, and foods. To demonstrate the utility of the model in a decision‐making context, we created a hypothetical case study and used it to compare different risk mitigation strategies for reducing contamination and spread of Listeria monocytogenes in a food facility. Model results indicated that areas with no direct contact with foods (e.g., loading dock and restroom) can serve as contamination niches and recontaminate areas that have direct contact with food products. Furthermore, food handlers’ behaviors, including, for example, hygiene and sanitation practices, can impact the persistence of microbial contamination in the facility environment and the spread of contamination to prepared foods. Using this case study, we also demonstrated benefits of an ABM framework for addressing food safety in a complex system in which emergent system‐level responses are predicted using a bottom‐up approach that observes individual agents (e.g., food handlers) and their behaviors. Our model can be applied to a wide variety of pathogens, food commodities, and activity patterns to evaluate efficacy of food‐safety management practices and quantify contamination reductions associated with proposed mitigation strategies in food facilities.     

A Mathematical Model for Pathogen Cross‐Contamination Dynamics during the Postharvest Processing of Leafy Greens

We developed a probabilistic mathematical model for the postharvest processing of leafy greens focusing on Escherichia coli O157:H7 contamination of fresh‐cut romaine lettuce as the case study. Our model can (i) support the investigation of cross‐contamination scenarios, and (ii) evaluate and compare different risk mitigation options. We used an agent‐based modeling framework to predict the pathogen prevalence and levels in bags of fresh‐cut lettuce and quantify spread of E. coli O157:H7 from contaminated lettuce to surface areas of processing equipment. Using an unbalanced factorial design, we were able to propagate combinations of random values assigned to model inputs through different processing steps and ranked statistically significant inputs with respect to their impacts on selected model outputs. Results indicated that whether contamination originated on incoming lettuce heads or on the surface areas of processing equipment, pathogen prevalence among bags of fresh‐cut lettuce and batches was most significantly impacted by the level of free chlorine in the flume tank and frequency of replacing the wash water inside the tank. Pathogen levels in bags of fresh‐cut lettuce were most significantly influenced by the initial levels of contamination on incoming lettuce heads or surface areas of processing equipment. The influence of surface contamination on pathogen prevalence or levels in fresh‐cut bags depended on the location of that surface relative to the flume tank. This study demonstrates that developing a flexible yet mathematically rigorous modeling tool, a “virtual laboratory,” can provide valuable insights into the effectiveness of individual and combined risk mitigation options.     

Modeling Growth and Reduction of Microorganisms in Foods as Functions of Temperature and Time

Food safety objectives (FSOs) are established in order to minimize the risk of foodborne illnesses to consumers, but these have not yet been incorporated into regulatory policy. An FSO states the maximum frequency and/or concentration of a microbiological hazard in a food at the time of consumption that provides an acceptable level of protection to the public and leads to a performance criterion for industry. However, in order to be implemented as a regulation, this criterion has to be achievable by the affected industry. In order to determine an FSO, the steps to produce and store that food need to be known, especially where they have an impact on contamination, growth, and destruction. This article uses existing models for growth of Listeria monocytogenes in conjunction with calculations of FSOs to approximate the outcome of more than one introduction of the foodborne organism throughout the food-processing path from the farm to the consumer. Most models for the growth and reduction of foodborne illnesses are logarithmic in nature, which fits the nature of the growth of microorganisms, spanning many orders of magnitude. However, these logarithmic models are normally limited to a single introduction step and a single reduction step. The model presented as part of this research addresses more than one introduction of food contamination, each of which can be separated by a substantial amount of time. The advantage of treating the problem this way is the accommodation of multiple introductions of foodborne pathogens over a range of time durations and conditions.     

Quantitative Risk Assessment of Human Salmonellosis in Canadian Broiler Chicken Breast from Retail to Consumption

The current quantitative risk assessment model followed the framework proposed by the Codex Alimentarius to provide an estimate of the risk of human salmonellosis due to consumption of chicken breasts which were bought from Canadian retail stores and prepared in Canadian domestic kitchens. The model simulated the level of Salmonella contamination on chicken breasts throughout the retail‐to‐table pathway. The model used Canadian input parameter values, where available, to represent risk of salmonellosis. From retail until consumption, changes in the concentration of Salmonella on each chicken breast were modeled using equations for growth and inactivation. The model predicted an average of 318 cases of salmonellosis per 100,000 consumers per year. Potential reasons for this overestimation were discussed. A sensitivity analysis showed that concentration of Salmonella on chicken breasts at retail and food hygienic practices in private kitchens such as cross‐contamination due to not washing cutting boards (or utensils) and hands after handling raw meat along with inadequate cooking contributed most significantly to the risk of human salmonellosis. The outcome from this model emphasizes that responsibility for protection from Salmonella hazard on chicken breasts is a shared responsibility. Data needed for a comprehensive Canadian Salmonella risk assessment were identified for future research.     

Quantitative Risk Assessment of Norovirus Transmission in Food Establishments: Evaluating the Impact of Intervention Strategies and Food Employee Behavior on the Risk Associated with Norovirus in Foods

We developed a quantitative risk assessment model using a discrete event framework to quantify and study the risk associated with norovirus transmission to consumers through food contaminated by infected food employees in a retail food setting. This study focused on the impact of ill food workers experiencing symptoms of diarrhea and vomiting and potential control measures for the transmission of norovirus to foods. The model examined the behavior of food employees regarding exclusion from work while ill and after symptom resolution and preventive measures limiting food contamination during preparation. The mean numbers of infected customers estimated for 21 scenarios were compared to the estimate for a baseline scenario representing current practices. Results show that prevention strategies examined could not prevent norovirus transmission to food when a symptomatic employee was present in the food establishment. Compliance with exclusion from work of symptomatic food employees is thus critical, with an estimated range of 75–226% of the baseline mean for full to no compliance, respectively. Results also suggest that efficient handwashing, handwashing frequency associated with gloving compliance, and elimination of contact between hands, faucets, and door handles in restrooms reduced the mean number of infected customers to 58%, 62%, and 75% of the baseline, respectively. This study provides quantitative data to evaluate the relative efficacy of policy and practices at retail to reduce norovirus illnesses and provides new insights into the interactions and interplay of prevention strategies and compliance in reducing transmission of foodborne norovirus.     

Integrated Approaches for the Public Health Prioritization of Foodborne and Zoonotic Pathogens

To address the persistent problems of foodborne and zoonotic disease, public health officials worldwide face difficult choices about how to best allocate limited resources and target interventions to reduce morbidity and mortality. Data‐driven approaches to informing these decisions have been developed in a number of countries. Integrated comparative frameworks generally share three methodological components: estimating incidence of acute illnesses, chronic sequelae, and mortality; attributing pathogen‐specific illnesses to foods; and calculating integrated measures of disease burden such as cost of illness, willingness to pay, and health‐adjusted life years (HALYs). To discuss the similarities and differences in these approaches, to seek consensus on principles, and to improve international collaboration, the E.U. MED‐VET‐NET and the U.S.‐based Food Safety Research Consortium organized an international conference convened in Berlin, Germany, on July 19–21, 2006. This article draws in part on the deliberations of the conference and discusses general principles, data needs, methodological issues and challenges, and future research needs pertinent to objective data‐driven analyses and their potential use for priority setting of foodborne and zoonotic pathogens in public health policy.     

The Bayesian Microbial Subtyping Attribution Model: Robustness to Prior Information and a Proposition

Attributing foodborne illnesses to food sources is essential to conceive, prioritize, and assess the impact of public health policy measures. The Bayesian microbial subtyping attribution model by Hald et al. is one of the most advanced approaches to attribute sporadic cases; it namely allows taking into account the level of exposure to the sources and the differences between bacterial types and between sources. This step forward requires introducing type and source‐dependent parameters, and generates overparameterization, which was addressed in Hald's paper by setting some parameters to constant values. We question the impact of the choices made for the parameterization (parameters set and values used) on model robustness and propose an alternative parameterization for the Hald model. We illustrate this analysis with the 2005 French data set of non‐typhi Salmonella. Mullner's modified Hald model and a simple deterministic model were used to compare the results and assess the accuracy of the estimates. Setting the parameters for bacterial types specific to a unique source instead of the most frequent one and using data‐based values instead of arbitrary values enhanced the convergence and adequacy of the estimates and led to attribution estimates consistent with the other models’ results. The type and source parameters estimates were also coherent with Mullner's model estimates. The model appeared to be highly sensitive to parameterization. The proposed solution based on specific types and data‐based values improved the robustness of estimates and enabled the use of this highly valuable tool successfully with the French data set.     

Development of a novel machine learning-based weighted modeling approach to incorporate Salmonella enterica heterogeneity on a genetic scale in a dose–response modeling framework

Estimating microbial dose–response is an important aspect of a food safety risk assessment. In recent years, there has been considerable interest to advance these models with potential incorporation of gene expression data. The aim of this study was to develop a novel machine learning model that considers the weights of expression of Salmonella genes that could be associated with illness, given exposure, in hosts. Here, an elastic net-based weighted Poisson regression method was proposed to identify Salmonella enterica genes that could be significantly associated with the illness response, irrespective of serovar. The best-fit elastic net model was obtained by 10-fold cross-validation. The best-fit elastic net model identified 33 gene expression–dose interaction terms that added to the predictability of the model. Of these, nine genes associated with Salmonella metabolism and virulence were found to be significant by the best-fit Poisson regression model (p < 0.05). This method could improve or redefine dose–response relationships for illness from relative proportions of significant genes from a microbial genetic dataset, which would help in refining endpoint and risk estimations.     

A Risk Assessment of Campylobacteriosis and Salmonellosis Linked to Chicken Meals Prepared in Households in Dakar,Senegal

We used a quantitative microbiological risk assessment model to describe the risk of Campylobacter and Salmonella infection linked to chicken meals prepared in households in Dakar, Senegal. The model uses data collected specifically for this study, such as the prevalence and level of bacteria on the neck skin of chickens bought in Dakar markets, time‐temperature profiles recorded from purchase to consumption, an observational survey of meal preparation in private kitchens, and detection and enumeration of pathogens on kitchenware and cooks’ hands. Thorough heating kills all bacteria present on chicken during cooking, but cross‐contamination of cooked chicken or ready‐to‐eat food prepared for the meal via kitchenware and cooks’ hands leads to a high expected frequency of pathogen ingestion. Additionally, significant growth of Salmonella is predicted during food storage at ambient temperature before and after meal preparation. These high exposures lead to a high estimated risk of campylobacteriosis and/or salmonellosis in Dakar households. The public health consequences could be amplified by the high level of antimicrobial resistance of Salmonella and Campylobacter observed in this setting. A significant decrease in the number of ingested bacteria and in the risk could be achieved through a reduction of the prevalence of chicken contamination at slaughter, and by the use of simple hygienic measures in the kitchen. There is an urgent need to reinforce the hygiene education of food handlers in Senegal.     

Risk Communication and Foodborne Illness: Message Sponsorship and Attempts to Stimulate Perceptions of Risk

Foodborne illness represents a serious health hazard in the United States. Since foodborne illness can often be prevented by an individual's behavior, messages aimed at promoting safe food-handling behaviors should be a major tool to reduce the incidence of foodborne illness. This article argues that to achieve adoption of safe food-handling practices in the home, food-safety messages should both stimulate risk perceptions and promote self-efficacy, feelings that one can successfully enact recommended behaviors. A content analysis of nationally distributed food-safety messages questioned if messages incorporated these features. Since food-safety communicators operate in complex environments with multiple and sometimes competing objectives, this study also questioned if sponsorship of foodborne illness prevention messages was related to the amount of content designed to alter risk perceptions associated with foodborne illness. Results of the quantitative content analysis found that copywriters generally included content designed to stimulate risk perception about foodborne illness but virtually ignored self-efficacy needs of the audience. A marked difference in tendencies to stimulate risk perceptions was found based on sponsorship. Both in volume and proportion, results show that governmentally sponsored messages more aggressively attempted to heighten risk perceptions associated with foodborne illness than did messages sponsored by privately funded communicators.     

Evaluation of Scenarios for Reducing Human Salmonellosis Through Household Consumption of Fresh Minced Pork Meat

Nontyphoidal salmonellosis is the second most frequently reported zoonotic disease in the European Union (EU) and is considered to be a major threat to human health worldwide. The most reported Salmonella serovar in the EU is S. Enteritidis, mainly associated with egg contamination, followed by S. Typhimurium, with the latter being the most predominant serovar isolated from pork. These findings suggest that reducing the Salmonella contamination in the pork production might be a good strategy to prevent and control human salmonellosis in the EU. Recently, a quantitative microbial risk assessment (QMRA) has been developed to assess the risks for human salmonellosis due to home consumption of fresh minced pork meat in Belgium.⁽ 1 ⁾ The newly developed risk model is called the METZOON model. In the current study, the METZOON model was used to evaluate the effectiveness of different hypothetical Salmonella mitigation strategies implemented at different stages of the minced pork production and consumption chain by means of a scenario analysis. To efficiently evaluate the mitigation strategies, model results were obtained by running simulations using the randomized complete block design. The effectiveness of a mitigation strategy is expressed using point and interval estimates of the effect size for dependent observations, expressed as the standardized difference in population means. The results indicate that the most effective strategies are taken during the slaughter processes of polishing, evisceration, and chilling, and during postprocessing, whereas interventions in the primary production and at the beginning of the slaughter process seem to have only a limited effect. Improving consumer awareness is found to be effective as well.     

Interventions Targeting Deep Tissue Lymph Nodes May Not Effectively Reduce the Risk of Salmonellosis from Ground Pork Consumption: A Quantitative Microbial Risk Assessment

The inclusion of deep tissue lymph nodes (DTLNs) or nonvisceral lymph nodes contaminated with Salmonella in wholesale fresh ground pork (WFGP) production may pose risks to public health. To assess the relative contribution of DTLNs to human salmonellosis occurrence associated with ground pork consumption and to investigate potential critical control points in the slaughter‐to‐table continuum for the control of human salmonellosis in the United States, a quantitative microbial risk assessment (QMRA) model was established. The model predicted an average of 45 cases of salmonellosis (95% CI = [19, 71]) per 100,000 Americans annually due to WFGP consumption. Sensitivity analysis of all stochastic input variables showed that cooking temperature was the most influential parameter for reducing salmonellosis cases associated with WFGP meals, followed by storage temperature and Salmonella concentration on contaminated carcass surface before fabrication. The input variables were grouped to represent three main factors along the slaughter‐to‐table chain influencing Salmonella doses ingested via WFGP meals: DTLN‐related factors, factors at processing other than DTLNs, and consumer‐related factors. The evaluation of the impact of each group of factors by second‐order Monte Carlo simulation showed that DTLN‐related factors had the lowest impact on the risk estimate among the three groups of factors. These findings indicate that interventions to reduce Salmonella contamination in DTLNs or to remove DTLNs from WFGP products may be less critical for reducing human infections attributable to ground pork than improving consumers’ cooking habits or interventions of carcass decontamination at processing.     

The potential for recall insurance to improve food safety

This paper explores the food safety implications of insurance products that compensate for business losses when food contamination causes a processing firm to initiate a recall. Discoveries of meat and poultry product contamination, in particular life-threatening pathogens, are increasing. The financial losses that follow a recall can be substantial as illustrated by several recent U.S. cases—Hudson Foods, Bil Mar, and Thorn Apple Valley Inc. Additionally, contaminated food product that escapes the current recall system poses a threat to consumer safety. The conceptual analysis presented here suggests that insurance underwriters could motivate earlier recalls and more diligent implementation of Hazard Analysis and Critical Control Point (HACCP). With sound underwriting, these changes could ultimately reduce the incidence of illness and death from foodborne pathogens.