Sara Monteiro Pires

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.

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.

Application of Bayesian Techniques to Model the Burden of Human Salmonellosis Attributable to U.S. Food Commodities at the Point of Processing: Adaptation of a Danish Model

Mathematical models that estimate the proportion of foodborne illnesses attributable to food commodities at specific points in the food chain may be useful to risk managers and policy makers to formulate public health goals, prioritize interventions, and document the effectiveness of mitigations aimed at reducing illness. Using human surveillance data on laboratory-confirmed Salmonella infections from the Centers for Disease Control and Prevention and Salmonella testing data from U.S. Department of Agriculture Food Safety and Inspection Services regulatory programs, we developed a point-of-processing foodborne illness attribution model by adapting the Hald Salmonella Bayesian source attribution model. Key model outputs include estimates of the relative proportions of domestically acquired sporadic human Salmonella infections resulting from contamination of raw meat, poultry, and egg products processed in the United States from 1998 through 2003. The current model estimates the relative contribution of chicken (48%), ground beef (28%), turkey (17%), egg products (6%), intact beef (1%), and pork (<1%) across 109 Salmonella serotypes found in food commodities at point of processing. While interpretation of the attribution estimates is constrained by data inputs, the adapted model shows promise and may serve as a basis for a common approach to attribution of human salmonellosis and food safety decision-making in more than one country.

Aetiology-Specific Estimates of the Global and Regional Incidence and Mortality of Diarrhoeal Diseases Commonly Transmitted through Food.

Background Diarrhoeal diseases are major contributors to the global burden of disease, particularly in children. However, comprehensive estimates of the incidence and mortality due to specific aetiologies of diarrhoeal diseases are not available. The objective of this study is to provide estimates of the global and regional incidence and mortality of diarrhoeal diseases caused by nine pathogens that are commonly transmitted through foods. Methods and Findings We abstracted data from systematic reviews and, depending on the overall mortality rates of the country, applied either a national incidence estimate approach or a modified Child Health Epidemiology Reference Group (CHERG) approach to estimate the aetiology-specific incidence and mortality of diarrhoeal diseases, by age and region. The nine diarrhoeal diseases assessed caused an estimated 1.8 billion (95% uncertainty interval [UI] 1.1–3.3 billion) cases and 599,000 (95% UI 472,000–802,000) deaths worldwide in 2010. The largest number of cases were caused by norovirus (677 million; 95% UI 468–1,153 million), enterotoxigenic Escherichia coli (ETEC) (233 million; 95% UI 154–380 million), Shigella spp. (188 million; 95% UI 94–379 million) and Giardia lamblia (179 million; 95% UI 125–263); the largest number of deaths were caused by norovirus (213,515; 95% UI 171,783–266,561), enteropathogenic E. coli (121,455; 95% UI 103,657–143,348), ETEC (73,041; 95% UI 55,474–96,984) and Shigella (64,993; 95% UI 48,966–92,357). There were marked regional differences in incidence and mortality for these nine diseases. Nearly 40% of cases and 43% of deaths caused by these nine diarrhoeal diseases occurred in children under five years of age. Conclusions Diarrhoeal diseases caused by these nine pathogens are responsible for a large disease burden, particularly in children. These aetiology-specific burden estimates can inform efforts to reduce diarrhoeal diseases caused by these nine pathogens commonly transmitted through foods.

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.

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.

Attributing foodborne salmonellosis in humans to animal reservoirs in the European Union using a multi-country stochastic model

A Bayesian modelling approach comparing the occurrence of Salmonella serovars in animals and humans was used to attribute salmonellosis cases to broilers, turkeys, pigs, laying hens, travel and outbreaks in 24 European Union countries. Salmonella data for animals and humans, covering the period from 2007 to 2009, were mainly obtained from studies and reports published by the European Food Safety Authority. Availability of food sources for consumption was derived from trade and production data from the European Statistical Office. Results showed layers as the most important reservoir of human salmonellosis in Europe, with 42·4% (7 903 000 cases, 95% credibility interval 4 181 000-14 510 000) of cases, 95·9% of which was caused by S. Enteritidis. In Finland and Sweden, most cases were travel-related, while in most other countries the main sources were related to the laying hen or pig reservoir, highlighting differences in the epidemiology of Salmonella, surveillance focus and eating habits across the European Union.

Attribution of human Listeria monocytogenes infections in England and Wales to ready-to-eat food sources placed on the market: adaptation of the Hald Salmonella source attribution model.

Human listeriosis is a rare but serious foodborne disease, with high morbidity and mortality in vulnerable populations (e.g., pregnant women, the elderly, and the immunocompromised). The disease is predominantly caused by the consumption of contaminated ready-to-eat foods. Since 2001, an increase in the number of listeriosis cases has been observed in several European Union countries, including England and Wales, predominantly in the over-60s population. The cause of this selective increased incidence is unknown. The Hald Salmonella Bayesian source attribution model was adapted to determine the potential of this approach to quantify the contribution of different food sources to the burden of human listeriosis in England and Wales from 2004 to 2007. The most important food sources for the overall population were multicomponent foods (sandwiches and prepacked mixed salad vegetables) (23.1%), finfish (16.8%), and beef (15.3%). Attribution of major sources of infection was similar for the elderly population (>or=60 years old, multicomponent foods [22.0%], finfish [14.7%], and beef [13.6%]). For pregnancy-associated cases, beef (12.3%), milk and milk products (11.8%), and finfish (11.2%) were more important sources of infection. The adapted model also showed that the serotype 4b was associated with relatively more human infections than that of other serotypes; further, the subtype 4b amplified fragment-length polymorphism V was associated with more pregnancy-associated cases than other subtypes of 4b. This approach of quantifying the contribution of various food sources to human listeriosis provides a useful tool in food safety risk analysis, and underlines the need for further emphasis to be given to the reduction of Listeria monocytogenes in high-risk foods, such as multicomponent foods, which are consumed without any further treatment. The need for targeted dietary advice for the elderly population is also highlighted.