Tine Hald

World Health Organization Estimates of the Global and Regional Disease Burden of 22 Foodborne Bacterial, Protozoal, and Viral Diseases, 2010: A Data Synthesis

Background Foodborne diseases are important worldwide, resulting in considerable morbidity and mortality. To our knowledge, we present the first global and regional estimates of the disease burden of the most important foodborne bacterial, protozoal, and viral diseases. Methods and Findings We synthesized data on the number of foodborne illnesses, sequelae, deaths, and Disability Adjusted Life Years (DALYs), for all diseases with sufficient data to support global and regional estimates, by age and region. The data sources included varied by pathogen and included systematic reviews, cohort studies, surveillance studies and other burden of disease assessments. We sought relevant data circa 2010, and included sources from 1990–2012. The number of studies per pathogen ranged from as few as 5 studies for bacterial intoxications through to 494 studies for diarrheal pathogens. To estimate mortality for Mycobacterium bovis infections and morbidity and mortality for invasive non-typhoidal Salmonella enterica infections, we excluded cases attributed to HIV infection. We excluded stillbirths in our estimates. We estimate that the 22 diseases included in our study resulted in two billion (95% uncertainty interval [UI] 1.5–2.9 billion) cases, over one million (95% UI 0.89–1.4 million) deaths, and 78.7 million (95% UI 65.0–97.7 million) DALYs in 2010. To estimate the burden due to contaminated food, we then applied proportions of infections that were estimated to be foodborne from a global expert elicitation. Waterborne transmission of disease was not included. We estimate that 29% (95% UI 23–36%) of cases caused by diseases in our study, or 582 million (95% UI 401–922 million), were transmitted by contaminated food, resulting in 25.2 million (95% UI 17.5–37.0 million) DALYs. Norovirus was the leading cause of foodborne illness causing 125 million (95% UI 70–251 million) cases, while Campylobacter spp. caused 96 million (95% UI 52–177 million) foodborne illnesses. Of all foodborne diseases, diarrheal and invasive infections due to non-typhoidal S. enterica infections resulted in the highest burden, causing 4.07 million (95% UI 2.49–6.27 million) DALYs. Regionally, DALYs per 100,000 population were highest in the African region followed by the South East Asian region. Considerable burden of foodborne disease is borne by children less than five years of age. Major limitations of our study include data gaps, particularly in middle- and high-mortality countries, and uncertainty around the proportion of diseases that were foodborne. Conclusions Foodborne diseases result in a large disease burden, particularly in children. Although it is known that diarrheal diseases are a major burden in children, we have demonstrated for the first time the importance of contaminated food as a cause. There is a need to focus food safety interventions on preventing foodborne diseases, particularly in low- and middle-income settings.

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.

Using outbreak data for source attribution of human salmonellosis and campylobacteriosis in Europe.

Salmonella and Campylobacter are the most important bacterial causes of foodborne illness in Europe. To identify and prioritize food safety interventions, it is important to quantify the burden of human foodborne illness attributable to specific sources. Data from outbreak investigations are observed at the public health endpoint and can therefore be a direct measure of attribution at the point of exposure. An analysis or summary of outbreak investigations is useful for attributing illnesses to foods, but often the implicated foods in reported outbreaks are complex foods, containing several food items, many of which could be the specific source of the infection. We describe a method that is able to attribute human cases to specific food items contained in complex foods. The model is based on data from investigations of Salmonella and Campylobacter outbreaks in the European Union in 2005 and 2006. The reporting of the causative vehicles for the outbreaks was not harmonized between and within countries. Consequently, we organized the implicated foods in mutually exclusive food categories. We estimated that the most important food sources for salmonellosis cases were eggs (32%) and meat and poultry-meat (15%), and that the majority of the cases of campylobacteriosis were attributed to chicken (10%). For both pathogens, a large proportion of cases could not be linked to any source. Among illnesses that could be attributed to a source, 58% of salmonellosis cases were attributed to eggs, and 29% of campylobacteriosis cases were attributed to chicken. Results also revealed regional differences in the relative importance of specific sources. We assessed the method to be of limited value to attribute human campylobacteriosis due to the limited number of outbreaks. Nevertheless, the presented source attribution approach can be applied to other foodborne pathogens, and is easily adaptable to countries having an appropriate number of reported outbreaks.

Source attribution of human campylobacteriosis using a meta-analysis of case-control studies of sporadic infections.

Campylobacter spp. is a widespread and important cause of human illness worldwide. Disease is frequently associated with foodborne transmission, but other routes of exposure, such as direct contact with live animals and person-to-person transmission, are also recognized. Identifying the most important sources of human disease is essential for prioritizing food safety interventions and setting public health goals. Numerous case-control studies of sporadic infections of campylobacteriosis have been published. These studies investigated a variety of potential risk factors for disease, often using different methodologies and settings. Systematic reviews (SRs) consist of a formal process for literature review focused on a specific research question, and include the identification of relevant literature, quality assessment of relevant studies, summarization or statistical analysis of data, and conclusions. With the objective of identifying the most important risk factors for human sporadic campylobacteriosis, we performed a SR of case-control studies of human sporadic cases and a meta-analysis of the obtained results. A combined SR focusing on Salmonella and Campylobacter studies was performed and the results analysed separately. From 1295 identified references, 131 passed the relevance screening, 73 passed the quality assessment stage, and data was extracted from 72 studies. Of these, 38 focused on campylobacteriosis. Information on exposures of cases and controls, and estimated odds ratios for investigated risk factors were collected and analysed. In the meta-analysis, heterogeneity between the studies and possible sources of bias were investigated, and pooled odds ratios for identified risk factors were estimated. Results suggest that travelling abroad, eating undercooked chicken, environmental sources, and direct contact with farm animals were significant risk factors for campylobacteriosis. Sub-analyses by geographical region, age group, and study period were performed, and differences were discussed.

The occurrence and epidemiology of Salmonella in European pig slaughterhouses

This study was part of an international research project entitled SALINPORK (FAIR CT-950400) initiated in 1996. The objectives were to investigate the occurrence of Salmonella in pig slaughterhouses and to identify risk factors associated with the contamination of pig carcasses. Data was collected from 12 slaughterhouses in five European countries. Isolates were characterized by serotyping, phage typing and antimicrobial susceptibility. In one country, no Salmonella was found. Salmonella was isolated from 5.3% of 3485 samples of pork and from 13.8% of 3573 environmental samples from the seven slaughterhouses in the four remaining countries. The statistical analyses (multi-level logistic regression) indicated that the prevalence was significantly higher during the warmer months and that the environmental contamination increased during the day of slaughter. The polishing (OR 3.74, 95% CI 1.43-9.78) and pluck removal (OR 3.63, 95% CI 1.66-7.96) processes were found to contribute significantly to the total carcass contamination, the latter especially if the scalding water also was contaminated. To reduce carcass contamination, it is recommended to ensure sufficiently high temperatures of scalding water (62 degrees C) and appropriate cleaning and disinfection of the polishing equipment at least once a day in order to reduce the level of carcass contamination and consequently the prevalence of Salmonella in pork.

Source Attribution of Human Salmonellosis: An Overview of Methods and Estimates

Reducing the burden of foodborne salmonellosis is challenging. It requires identification of the most important food sources causing disease and prioritization of effective intervention strategies. For this purpose, a variety of methods to estimate the relative contribution of different sources of Salmonella infections have been applied worldwide. Each has strengths and limitations, and the usefulness of each depends on the public health questions being addressed. In this study, we reviewed the source attribution methods and outcomes of several studies developed in different countries and settings, comparing approaches and regional differences in attribution estimates. Reviewed results suggest that illnesses and outbreaks are most commonly attributed to exposure to contaminated food, and that eggs, broiler chickens, and pigs are among the top sources. Although most source attribution studies do not attribute salmonellosis to produce, outbreak data in several countries suggest that exposure to raw vegetables is also an important source. International travel was also a consistently important exposure in several studies. Still, the relative contribution of specific sources to human salmonellosis varied substantially between studies. Although differences in data inputs, methods, and the point in the food system where attribution was estimated contribute to variability between studies, observed differences also suggest regional differences in the epidemiology of salmonellosis.

Attributing human foodborne illness to food sources and water in Latin America and the Caribbean using data from outbreak investigations

Foodborne pathogens are responsible for an increasing burden of disease worldwide. Knowledge on the contribution of different food sources and water for disease is essential to prioritize food safety interventions and implement appropriate control measures. Source attribution using outbreak data utilizes readily available data from outbreak surveillance to estimate the contribution of different sources to human disease. We developed a probabilistic model based on outbreak data that attributes human foodborne disease by various bacterial pathogens to sources in Latin America and the Caribbean (LA&C). Foods implicated in outbreaks were classified by their ingredients as simple foods (i.e. belonging to one single food category), or complex foods (i.e. belonging to multiple food categories). For each agent, the data from simple-food outbreaks were summarized, and the proportion of outbreaks caused by each category was used to define the probability that an outbreak was caused by a source. For the calculation of the number of outbreaks attributed to each source, simple-food outbreaks were attributed to the single food category in question, and complex-food outbreaks were partitioned to each category proportionally to the estimated probability. We analysed all bacterial pathogens together, focused on important bacterial pathogens separately, and, when data were sufficient, performed analyses by country, decade and location. Between 1993 and 2010, 6313 bacterial outbreaks were reported by 20 countries. In general, the most important sources of bacterial disease were meat, dairy products, water and vegetables in the 1990s, and eggs, vegetables, and grains and beans in the 2000s. We observed fluctuations of the most important sources of disease for each pathogen between decades and countries, which may be a consequence of changes in the control of zoonotic disease over the years, of changes in food consumption habits, or of changes in public health focus and availability of data of different pathogens. This study identified data gaps in the region and highlighted the importance of effective surveillance systems to identify sources of disease. Still, the application of this method for source attribution in the LA&C region was successful, and we concluded that this approach can be used to attribute disease to food sources and water in other regions, including developing regions with limited data on the public health impact of foodborne diseases.

WHO Initiative to Estimate the Global Burden of Foodborne Diseases

Abstract Background The public health impact of foodborne diseases globally is unknown. The WHO Initiative to Estimate the Global Burden of Foodborne Diseases was launched out of the need to fill this data gap. It is anticipated that this effort will enable policy makers and other stakeholders to set appropriate, evidence-informed priorities in the area of food safety. Methods The Initiative aims to provide estimates on the global burden of foodborne diseases by age, sex, and region; strengthen country capacity for conducting burden of foodborne disease assessments in parallel with food safety policy analyses; increase awareness and commitment among Member States for the implementation of food safety policy and standards; and encourage countries to use burden of foodborne disease estimates for cost-effectiveness analyses of prevention, intervention, and control measures. To estimate the global burden (expressed in disability-adjusted life-years), the Foodborne Disease Burden Epidemiology Reference Group (FERG) focused on the contamination of food with enteric and parasitic pathogens, chemicals, and toxins. Findings Study findings will provide the technical background and challenges of assessing the burden of foodborne diseases, based on national and international studies. Systematic reviews to support estimates of the incidence and mortality of food-related diseases are being completed. Results will be used to update and refine global burden estimates for relevant food-related hazards, in the context of other international burden of disease studies. It is recognised that exposure to such hazards may also occur through other pathways including the environment (eg, water, air) and by direct transmission (eg, human-to-human and animal-to-human). Structured expert elicitation will be used to provide the basis for attribution of incidence and burden to food, and estimation of the most important food sources. Interpretation Estimating the global burden of foodborne diseases is highly complex because of the diversity of hazards that can be transmitted by food, the multitude of health outcomes they cause, and complex transmission pathways. WHO is planning to present a global estimate for the first time in 2014. Funding WHO.

Association Between Antimicrobial Resistance in Escherichia coli Isolates from Food Animals and Blood Stream Isolates from Humans in Europe: An Ecological Study

BACKGROUND In addition to medical antimicrobial usage, the use of antimicrobials in food animals contributes to the occurrence of resistance among some bacterial species isolated from infections in humans. Recently, several studies have indicated that a large proportion of Escherichia coli causing infections in humans, especially those resistant to antimicrobials, have an animal origin. METHODS We analyzed the correlation between the prevalence of antimicrobial resistance in E. coli isolates from blood stream infections in humans and in E. coli isolates from poultry, pigs, and cattle between 2005 and 2008 for 11 countries, using available surveillance data. We also assessed the correlation between human antimicrobial usage and the occurrence of resistance in E. coli isolates from blood stream infections. RESULTS Strong and significant correlations between prevalences of resistance to ampicillin (r=0.94), aminoglycosides (r=0.72), third-generation cephalosporins (r=0.76), and fluoroquinolones (r=0.68) were observed for human and poultry E. coli isolates. Similar significant correlations were observed for ampicillin (r=0.91), aminoglycosides (r=0.73), and fluoroquinolone resistance (r=0.74) in pig and human isolates. In cattle isolates, only ampicillin resistance (r=0.72) was significantly correlated to human isolates. When usage of antimicrobials in humans was analyzed with antimicrobial resistance among human isolates, only correlations between fluoroquinolones (r=0.90) and third-generation cephalosporins (r=0.75) were significant. CONCLUSIONS Resistance in E. coli isolates from food animals (especially poultry and pigs) was highly correlated with resistance in isolates from humans. This supports the hypothesis that a large proportion of resistant E. coli isolates causing blood stream infections in people may be derived from food sources.

Assessing the differences in public health impact of Salmonella subtypes using a Bayesian microbial subtyping approach for source attribution.

Salmonella is a major cause of human gastroenteritis worldwide. To prioritize interventions and assess the effectiveness of efforts to reduce illness, it is important to attribute salmonellosis to the responsible sources. Studies have suggested that some Salmonella subtypes have a higher health impact than others. Likewise, some food sources appear to have a higher impact than others. Knowledge of variability in the impact of subtypes and sources may provide valuable added information for research, risk management, and public health strategies. We developed a Bayesian model that attributes illness to specific sources and allows for a better estimation of the differences in the ability of Salmonella subtypes and food types to result in reported salmonellosis. The model accommodates data for multiple years and is based on the Danish Salmonella surveillance. The number of sporadic cases caused by different Salmonella subtypes is estimated as a function of the prevalence of these subtypes in the animal-food sources, the amount of food consumed, subtype-related factors, and source-related factors. Our results showed relative differences between Salmonella subtypes in their ability to cause disease. These differences presumably represent multiple factors, such as differences in survivability through the food chain and/or pathogenicity. The relative importance of the source-dependent factors varied considerably over the years, reflecting, among others, variability in the surveillance programs for the different animal sources. The presented model requires estimation of fewer parameters than a previously developed model, and thus allows for a better estimation of these factors to result in reported human disease. In addition, a comparison of the results of the same model using different sets of typing data revealed that the model can be applied to data with less discriminatory power, which is the only data available in many countries. In conclusion, the model allows for the estimation of relative differences between Salmonella subtypes and sources, providing results that will benefit future risk assessment or risk ranking purposes.