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

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          Abstract

          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.

          Abstract

          In this data synthesis, Martyn Kirk and colleagues estimate the global and regional disease burden of 22 foodborne bacterial, protozoal and viral diseases.

          Editors' Summary

          Background

          Foodborne diseases are responsible for a large burden of illness (morbidity) and death (mortality) in both resource-rich and resource-poor countries. More than 200 diseases can be transmitted to people through the ingestion of food contaminated with microorganisms (bacteria, viruses, and parasites) or with chemicals. Contamination of food can occur at any stage of food production—on farms where crops are grown and animals raised, in factories where food is processed, and during food storage and preparation in shops, restaurants and the home. Contamination can arise because of pollution of the water, soil or air or through poor food-handling practices such as failing to wash one’s hands before preparing food. Many foodborne diseases (for example, norovirus, Escherichia coli, and campylobacter infections) present with gastrointestinal symptoms—stomach cramps, diarrhea, and vomiting. However, some foodborne illnesses cause symptoms affecting other parts of the body and some have serious sequelae (abnormal bodily conditions or diseases arising from a pre-existing disease). For example, infection with some strains of E. coli can lead to kidney failure.

          Why Was This Study Done?

          Accurate regional and global estimates of the disease burden of foodborne illnesses are needed to guide governmental and international efforts to improve food safety. However, estimates of the number of cases of foodborne illness, sequelae, deaths, and disability adjusted life years (a DALY represents the disease-related loss of one year of full health because of premature death or disability; DALYs provide a measure of the burden of a disease) are only available for a few countries. Consequently, in 2007, the World Health Organization (WHO) established the Foodborne Disease Burden Epidemiology Reference Group (FERG) to estimate the global and regional burden of disease attributable to foodborne illnesses. Here, researchers involved in one of the constituent task forces of FERG—the Enteric Diseases Task Force—undertake a data synthesis (the combination of information from many different sources) to provide global and regional estimates of the disease burden of several important foodborne bacterial, protozoal (parasitic), and viral diseases.

          What Did the Researchers Do and Find?

          The researchers combined national estimates of foodborne diseases and data from systematic reviews (studies that identify all the research on a given topic using predefined criteria), national surveillance programs, and other sources to estimate the number of illnesses, sequelae, deaths and DALYs globally and regionally for 22 diseases with sufficient data to support such estimations. Together, these 17 bacterial infections, two viral infections, and three protozoal infections caused 2 billion cases of illness, more than 1 million deaths, and almost 80 million DALYs in 2010. Using information on the proportions of infections considered to be foodborne by expert panels, the researchers estimated that nearly a third of these cases of illness (582 million cases), resulting in 25 million DALYs, were transmitted by contaminated food. Notably, 38% of the cases of foodborne illness, 33% of deaths from these diseases, and 43% of the disease burden from contaminated food (11 million DALYs) occurred in children under 5 years old. The leading cause of foodborne illness was norovirus (125 million cases), closely followed by campylobacter (96 million); diarrheal and invasive infections caused by non-typhoidal Salmonella enterica infections caused the largest burden of disease (4.07 million DALYs). Finally, the burden of foodborne illness was highest in WHO’s African region.

          What Do These Findings Mean?

          The lack of reliable data on the 22 illnesses considered in this analysis for many regions of the world, including some of the most populous regions, and uncertainty about the proportion of the cases of each illness that is foodborne may limit the accuracy of these findings. Nevertheless, these results provide new information about the regional and global disease burden caused by foodborne illnesses. In particular, these estimates reveal an unexpectedly high disease burden caused by foodborne illnesses among young children. Thus, although children under the age of 5 years represent only 9% of the global population, nearly half of the disease burden from contaminated food may occur in this age group. Overall, the findings of this study suggest that governments and international agencies should prioritize food safety to prevent foodborne illness, particularly among young children, and highlight the need to identify effective food hygiene interventions that can be implemented in low- and middle-income countries.

          Additional Information

          This list of resources contains links that can be accessed when viewing the PDF on a device or via the online version of the article at http://dx.doi.org/10.1371/journal.pmed.1001921.

          Related collections

          Most cited references28

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          The global burden of nontyphoidal Salmonella gastroenteritis.

          To estimate the global burden of nontyphoidal Salmonella gastroenteritis, we synthesized existing data from laboratory-based surveillance and special studies, with a hierarchical preference to (1) prospective population-based studies, (2) "multiplier studies," (3) disease notifications, (4) returning traveler data, and (5) extrapolation. We applied incidence estimates to population projections for the 21 Global Burden of Disease regions to calculate regional numbers of cases, which were summed to provide a global number of cases. Uncertainty calculations were performed using Monte Carlo simulation. We estimated that 93.8 million cases (5th to 95th percentile, 61.8-131.6 million) of gastroenteritis due to Salmonella species occur globally each year, with 155,000 deaths (5th to 95th percentile, 39,000-303,000 deaths). Of these, we estimated 80.3 million cases were foodborne. Salmonella infection represents a considerable burden in both developing and developed countries. Efforts to reduce transmission of salmonellae by food and other routes must be implemented on a global scale.
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            GBD 2010: design, definitions, and metrics.

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              Is Open Access

              Global Causes of Diarrheal Disease Mortality in Children <5 Years of Age: A Systematic Review

              Estimation of pathogen-specific causes of child diarrhea deaths is needed to guide vaccine development and other prevention strategies. We did a systematic review of articles published between 1990 and 2011 reporting at least one of 13 pathogens in children <5 years of age hospitalized with diarrhea. We included 2011 rotavirus data from the Rotavirus Surveillance Network coordinated by WHO. We excluded studies conducted during diarrhea outbreaks that did not discriminate between inpatient and outpatient cases, reporting nosocomial infections, those conducted in special populations, not done with adequate methods, and rotavirus studies in countries where the rotavirus vaccine was used. Age-adjusted median proportions for each pathogen were calculated and applied to 712 000 deaths due to diarrhea in children under 5 years for 2011, assuming that those observed among children hospitalized for diarrhea represent those causing child diarrhea deaths. 163 articles and WHO studies done in 31 countries were selected representing 286 inpatient studies. Studies seeking only one pathogen found higher proportions for some pathogens than studies seeking multiple pathogens (e.g. 39% rotavirus in 180 single-pathogen studies vs. 20% in 24 studies with 5–13 pathogens, p<0·0001). The percentage of episodes for which no pathogen could be identified was estimated to be 34%; the total of all age-adjusted percentages for pathogens and no-pathogen cases was 138%. Adjusting all proportions, including unknowns, to add to 100%, we estimated that rotavirus caused 197 000 [Uncertainty range (UR) 110 000–295 000], enteropathogenic E. coli 79 000 (UR 31 000–146 000), calicivirus 71 000 (UR 39 000–113 000), and enterotoxigenic E. coli 42 000 (UR 20 000–76 000) deaths. Rotavirus, calicivirus, enteropathogenic and enterotoxigenic E. coli cause more than half of all diarrheal deaths in children <5 years in the world.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS Med
                PLoS Med
                plos
                plosmed
                PLoS Medicine
                Public Library of Science (San Francisco, CA USA )
                1549-1277
                1549-1676
                3 December 2015
                December 2015
                : 12
                : 12
                : e1001921
                Affiliations
                [1 ]The Australian National University, Canberra, Australia
                [2 ]Danish Technical University, Copenhagen, Denmark
                [3 ]Johns Hopkins University, Baltimore, Maryland, United States of America
                [4 ]Food and Agriculture Organization, Rome, Italy
                [5 ]Centre for International Health, University of Otago, Dunedin, New Zealand
                [6 ]Ghent University, Merelbeke, Belgium
                [7 ]Université catholique de Louvain, Brussels, Belgium
                [8 ]Institute of Tropical Medicine, Antwerp, Belgium
                [9 ]University of Wisconsin, Madison, Madison, Wisconsin, United States of America
                [10 ]Public Health Agency of Canada, Guelph, Ontario, Canada
                [11 ]Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America
                [12 ]Centre for Enteric Diseases, National Institute for Communicable Diseases, and Faculty of Health Sciences, University of Witwatersrand, Johannesburg, South Africa
                [13 ]Institute of Environmental Science and Research, Christchurch, New Zealand
                [14 ]Instituto de Investigación Nutricional, Lima, Peru
                [15 ]US Naval Medical Research Unit No. 6, Callao, Peru
                [16 ]University of Zürich, Zürich, Switzerland
                [17 ]National Institute for Public Health and the Environment, Bilthoven, The Netherlands
                [18 ]University of Florida, Gainesville, Gainesville, Florida, United States of America
                [19 ]Utrecht University, Utrecht, The Netherlands
                Mahidol-Oxford Tropical Medicine Research Unit, THAILAND
                Author notes

                The findings and conclusions of this report are those of the authors and do not necessarily represent the official views, decisions or policies of the World Health Organization, US Centers for Disease Control and Prevention, the Department of the Navy, Department of Defense, the US Government or other institutions listed. CFL, AJH, and FJA are employees of the US Government. MDK, REB, MC, BD, DD, AF, TH, KHK, RL, CFL, PRT, AHH, and FJA serve as members of the World Health Organization advisory body—the Foodborne Disease Epidemiology Reference Group—without remuneration. MDK is a member of the Editorial Board for PLOS ONE. PRT is a member of the Editorial Board for PLOS Neglected Tropical Diseases.

                Conceived and designed the experiments: MDK SMP REB BD DD AF CLFW TH KHK RL CFL PRT AHH FJA. Performed the experiments: SMP JAC BD CLFW TH AJH CFL FJA. Analyzed the data: MDK SMP JAC BD CLFW TH AJH CFL FJA. Wrote the first draft of the manuscript: FJA MDK. Contributed to the writing of the manuscript: MDK SMP REB MC JAC BD DD AF CLFW TH AJH KHK RL CFL PRT AHH FJA. Agree with the manuscript’s results and conclusions: MDK SMP REB MC JAC BD DD AF CLFW TH AJH KHK RL CFL PRT AHH FJA. All authors have read, and confirm that they meet, ICMJE criteria for authorship.

                Article
                PMEDICINE-D-15-00862
                10.1371/journal.pmed.1001921
                4668831
                26633831
                16b7dc39-9071-41df-8341-811aa27fcbcb

                2015 World Health Organization. This is an open access article distributed under the Creative Commons Attribution IGO License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. http://creativecommons.org/licenses/by/3.0/igo/. This article should not be reproduced for use in association with the promotion of commercial products, services or any legal entity.

                History
                : 20 March 2015
                : 3 November 2015
                Page count
                Figures: 1, Tables: 4, Pages: 21
                Funding
                This study was commissioned and paid for by the World Health Organization (WHO). Copyright in the original work on which this article is based belongs to WHO. The authors have been given permission to publish this article. We acknowledge the support from the Bill & Melinda Gates Foundation that funded CFL, CFW, and REB through the Child Health Epidemiology Reference Group (CHERG). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

                Medicine
                Medicine

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