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      Attribution of country level foodborne disease to food group and food types in three African countries: Conclusions from a structured expert judgment study

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          Abstract

          Background

          According to the World Health Organization, 600 million cases of foodborne disease occurred in 2010. To inform risk management strategies aimed at reducing this burden, attribution to specific foods is necessary.

          Objective

          We present attribution estimates for foodborne pathogens ( Campylobacter spp., enterotoxigenic Escherichia coli (ETEC), Shiga-toxin producing E. coli, nontyphoidal Salmonella enterica, Cryptosporidium spp., Brucella spp., and Mycobacterium bovis) in three African countries (Burkina Faso, Ethiopia, Rwanda) to support risk assessment and cost-benefit analysis in three projects aimed at increasing safety of beef, dairy, poultry meat and vegetables in these countries.

          Methods

          We used the same methodology as the World Health Organization, i.e., Structured Expert Judgment according to Cooke’s Classical Model, using three different panels for the three countries. Experts were interviewed remotely and completed calibration questions during the interview without access to any resources. They then completed target questions after the interview, using resources as considered necessary. Expert data were validated using two objective measures, calibration score or statistical accuracy, and information score. Performance-based weights were derived from the two measures to aggregate experts’ distributions into a so-called decision maker. The analysis was made using Excalibur software, and resulting distributions were normalized using Monte Carlo simulation.

          Results

          Individual experts’ uncertainty assessments resulted in modest statistical accuracy and high information scores, suggesting overconfident assessments. Nevertheless, the optimized item-weighted decision maker was statistically accurate and informative. While there is no evidence that animal pathogenic ETEC strains are infectious to humans, a sizeable proportion of ETEC illness was attributed to animal source foods as experts considered contamination of food products by infected food handlers can occur at any step in the food chain. For all pathogens, a major share of the burden was attributed to food groups of interest. Within food groups, the highest attribution was to products consumed raw, but processed products were also considered important sources of infection.

          Conclusions

          Cooke’s Classical Model with performance-based weighting provided robust uncertainty estimates of the attribution of foodborne disease in three African countries. Attribution estimates will be combined with country-level estimates of the burden of foodborne disease to inform decision making by national authorities.

          Author summary

          The World Health Organization has presented estimates of the burden of foodborne disease and attribution percentages of zoonotic foodborne pathogens to food groups (e.g., beef, vegetables). To inform food safety decision making at the national level, these estimates should be combined, extended to pathogens with human reservoirs and provided at a more detailed level (e.g., drinking raw milk as one food product in the dairy group). We present a Structured Expert Elicitation study using the same protocol as the World Health Organization (Cooke’s Classical Model) to attribute foodborne disease of selected pathogens ( Campylobacter spp., enterotoxigenic Escherichia coli, Shiga-toxin producing E. coli, nontyphoidal Salmonella enterica, Cryptosporidium spp., Brucella spp., Mycobacterium bovis) to different food types and food products in the beef, dairy, poultry and vegetable groups in three African countries (Burkina Faso, Ethiopia, and Rwanda). Individual experts’ uncertainty assessments resulted in modest statistical accuracy and high information scores, that is concentrated in small ranges, suggesting overconfident assessments. Nevertheless, the optimized item-weighted decision maker was statistically accurate and informative. Cooke’s Classical Model with performance-based weighting provided robust uncertainty estimates of the attribution of foodborne disease in three African countries.

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          Most cited references12

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          World Health Organization Global Estimates and Regional Comparisons of the Burden of Foodborne Disease in 2010

          Illness and death from diseases caused by contaminated food are a constant threat to public health and a significant impediment to socio-economic development worldwide. To measure the global and regional burden of foodborne disease (FBD), the World Health Organization (WHO) established the Foodborne Disease Burden Epidemiology Reference Group (FERG), which here reports their first estimates of the incidence, mortality, and disease burden due to 31 foodborne hazards. We find that the global burden of FBD is comparable to those of the major infectious diseases, HIV/AIDS, malaria and tuberculosis. The most frequent causes of foodborne illness were diarrheal disease agents, particularly norovirus and Campylobacter spp. Diarrheal disease agents, especially non-typhoidal Salmonella enterica, were also responsible for the majority of deaths due to FBD. Other major causes of FBD deaths were Salmonella Typhi, Taenia solium and hepatitis A virus. The global burden of FBD caused by the 31 hazards in 2010 was 33 million Disability Adjusted Life Years (DALYs); children under five years old bore 40% of this burden. The 14 subregions, defined on the basis of child and adult mortality, had considerably different burdens of FBD, with the greatest falling on the subregions in Africa, followed by the subregions in South-East Asia and the Eastern Mediterranean D subregion. Some hazards, such as non-typhoidal S. enterica, were important causes of FBD in all regions of the world, whereas others, such as certain parasitic helminths, were highly localised. Thus, the burden of FBD is borne particularly by children under five years old–although they represent only 9% of the global population–and people living in low-income regions of the world. These estimates are conservative, i.e., underestimates rather than overestimates; further studies are needed to address the data gaps and limitations of the study. Nevertheless, all stakeholders can contribute to improvements in food safety throughout the food chain by incorporating these estimates into policy development at national and international levels.
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            Selected major risk factors and global and regional burden of disease.

            Reliable and comparable analysis of risks to health is key for preventing disease and injury. Causal attribution of morbidity and mortality to risk factors has traditionally been in the context of individual risk factors, often in a limited number of settings, restricting comparability. Our aim was to estimate the contributions of selected major risk factors to global and regional burden of disease in a unified framework. For 26 selected risk factors, expert working groups undertook a comprehensive review of published work and other sources--eg, government reports and international databases--to obtain data on the prevalence of risk factor exposure and hazard size for 14 epidemiological regions of the world. Population attributable fractions were estimated by applying the potential impact fraction relation, and applied to the mortality and burden of disease estimates from the global burden of disease (GBD) database. Childhood and maternal underweight (138 million disability adjusted life years [DALY], 9.5%), unsafe sex (92 million DALY, 6.3%), high blood pressure (64 million DALY, 4.4%), tobacco (59 million DALY, 4.1%), and alcohol (58 million DALY, 4.0%) were the leading causes of global burden of disease. In the poorest regions of the world, childhood and maternal underweight, unsafe sex, unsafe water, sanitation, and hygiene, indoor smoke from solid fuels, and various micronutrient deficiencies were major contributors to loss of healthy life. In both developing and developed regions, alcohol, tobacco, high blood pressure, and high cholesterol were major causes of disease burden. Substantial proportions of global disease burden are attributable to these major risks, to an extent greater than previously estimated. Developing countries suffer most or all of the burden due to many of the leading risks. Strategies that target these known risks can provide substantial and underestimated public-health gains.
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              World Health Organization Estimates of the Relative Contributions of Food to the Burden of Disease Due to Selected Foodborne Hazards: A Structured Expert Elicitation

              Background The Foodborne Disease Burden Epidemiology Reference Group (FERG) was established in 2007 by the World Health Organization (WHO) to estimate the global burden of foodborne diseases (FBDs). This estimation is complicated because most of the hazards causing FBD are not transmitted solely by food; most have several potential exposure routes consisting of transmission from animals, by humans, and via environmental routes including water. This paper describes an expert elicitation study conducted by the FERG Source Attribution Task Force to estimate the relative contribution of food to the global burden of diseases commonly transmitted through the consumption of food. Methods and Findings We applied structured expert judgment using Cooke’s Classical Model to obtain estimates for 14 subregions for the relative contributions of different transmission pathways for eleven diarrheal diseases, seven other infectious diseases and one chemical (lead). Experts were identified through international networks followed by social network sampling. Final selection of experts was based on their experience including international working experience. Enrolled experts were scored on their ability to judge uncertainty accurately and informatively using a series of subject-matter specific ‘seed’ questions whose answers are unknown to the experts at the time they are interviewed. Trained facilitators elicited the 5th, and 50th and 95th percentile responses to seed questions through telephone interviews. Cooke’s Classical Model uses responses to the seed questions to weigh and aggregate expert responses. After this interview, the experts were asked to provide 5th, 50th, and 95th percentile estimates for the ‘target’ questions regarding disease transmission routes. A total of 72 experts were enrolled in the study. Ten panels were global, meaning that the experts should provide estimates for all 14 subregions, whereas the nine panels were subregional, with experts providing estimates for one or more subregions, depending on their experience in the region. The size of the 19 hazard-specific panels ranged from 6 to 15 persons with several experts serving on more than one panel. Pathogens with animal reservoirs (e.g. non-typhoidal Salmonella spp. and Toxoplasma gondii) were in general assessed by the experts to have a higher proportion of illnesses attributable to food than pathogens with mainly a human reservoir, where human-to-human transmission (e.g. Shigella spp. and Norovirus) or waterborne transmission (e.g. Salmonella Typhi and Vibrio cholerae) were judged to dominate. For many pathogens, the foodborne route was assessed relatively more important in developed subregions than in developing subregions. The main exposure routes for lead varied across subregions, with the foodborne route being assessed most important only in two subregions of the European region. Conclusions For the first time, we present worldwide estimates of the proportion of specific diseases attributable to food and other major transmission routes. These findings are essential for global burden of FBD estimates. While gaps exist, we believe the estimates presented here are the best current source of guidance to support decision makers when allocating resources for control and intervention, and for future research initiatives.
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                Author and article information

                Contributors
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: Writing – original draft
                Role: InvestigationRole: MethodologyRole: Writing – original draft
                Role: ConceptualizationRole: Funding acquisitionRole: Project administrationRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: MethodologyRole: SoftwareRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                12 September 2022
                September 2022
                : 16
                : 9
                : e0010663
                Affiliations
                [1 ] Emerging Pathogens Institute, Food Systems Institute, Animal Sciences Department, University of Florida, Gainesville, Florida, United States of America
                [2 ] Delft Institute of Applied Mathematics, Delft University of Technology, Delft, The Netherlands
                George Washington University Medical Center, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                [¤]

                Current address: Abrams Public Health Center, Tucson, Arizona, United States of America

                Author information
                https://orcid.org/0000-0002-6456-5460
                Article
                PNTD-D-22-00143
                10.1371/journal.pntd.0010663
                9499278
                36094953
                fae7bff1-5f36-4936-bdf7-8f2692ccc343
                © 2022 Sapp et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 31 January 2022
                : 14 July 2022
                Page count
                Figures: 7, Tables: 8, Pages: 21
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100000617, Foreign and Commonwealth Office;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000865, Bill and Melinda Gates Foundation;
                Award ID: OPP1195588; OPP1195643
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100006928, Ohio State University;
                Award ID: OPP1195643, TARTARE
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000200, United States Agency for International Development;
                Award ID: AID-OAA-L-15-00003
                Award Recipient :
                o ACS, MPA and AHH were funded by the UK Foreign, Commonwealth & Development Office (FCDO), the Bill & Melinda Gates Foundation and the CGIAR Research Program on Agriculture for Nutrition and Health led by the International Food Policy Research Institute through a project entitled “Urban food markets in Africa: Incentivizing food safety using a pull-push approach” (OPP1195588, The Pull-Push Project) and a project led by the Ohio State University entitled “The Assessment and Management of Risk from Non-typhoidal Salmonella, Diarrheagenic Escherichia coli and Campylobacter in Raw Beef and Dairy in Ethiopia” (OPP1195643, TARTARE) and the United States Agency for International Development (USAID) Bureau for Food Security under Agreement # AID-OAA-L-15-00003 as part of Feed the Future Innovation Lab for Livestock Systems. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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