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      World Health Organization Estimates of the Global and Regional Disease Burden of 11 Foodborne Parasitic Diseases, 2010: A Data Synthesis

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          Abstract

          Background

          Foodborne diseases are globally important, resulting in considerable morbidity and mortality. Parasitic diseases often result in high burdens of disease in low and middle income countries and are frequently transmitted to humans via contaminated food. This study presents the first estimates of the global and regional human disease burden of 10 helminth diseases and toxoplasmosis that may be attributed to contaminated food.

          Methods and Findings

          Data were abstracted from 16 systematic reviews or similar studies published between 2010 and 2015; from 5 disease data bases accessed in 2015; and from 79 reports, 73 of which have been published since 2000, 4 published between 1995 and 2000 and 2 published in 1986 and 1981. These included reports from national surveillance systems, journal articles, and national estimates of foodborne diseases. These data were used to estimate the number of infections, sequelae, deaths, and Disability Adjusted Life Years (DALYs), by age and region for 2010. These parasitic diseases, resulted in 48.4 million cases (95% Uncertainty intervals [UI] of 43.4–79.0 million) and 59,724 (95% UI 48,017–83,616) deaths annually resulting in 8.78 million (95% UI 7.62–12.51 million) DALYs. We estimated that 48% (95% UI 38%-56%) of cases of these parasitic diseases were foodborne, resulting in 76% (95% UI 65%-81%) of the DALYs attributable to these diseases. Overall, foodborne parasitic disease, excluding enteric protozoa, caused an estimated 23.2 million (95% UI 18.2–38.1 million) cases and 45,927 (95% UI 34,763–59,933) deaths annually resulting in an estimated 6.64 million (95% UI 5.61–8.41 million) DALYs. Foodborne Ascaris infection (12.3 million cases, 95% UI 8.29–22.0 million) and foodborne toxoplasmosis (10.3 million cases, 95% UI 7.40–14.9 million) were the most common foodborne parasitic diseases. Human cysticercosis with 2.78 million DALYs (95% UI 2.14–3.61 million), foodborne trematodosis with 2.02 million DALYs (95% UI 1.65–2.48 million) and foodborne toxoplasmosis with 825,000 DALYs (95% UI 561,000–1.26 million) resulted in the highest burdens in terms of DALYs, mainly due to years lived with disability. Foodborne enteric protozoa, reported elsewhere, resulted in an additional 67.2 million illnesses or 492,000 DALYs. Major limitations of our study include often substantial data gaps that had to be filled by imputation and suffer from the uncertainties that surround such models. Due to resource limitations it was also not possible to consider all potentially foodborne parasites (for example Trypanosoma cruzi).

          Conclusions

          Parasites are frequently transmitted to humans through contaminated food. These estimates represent an important step forward in understanding the impact of foodborne diseases globally and regionally. The disease burden due to most foodborne parasites is highly focal and results in significant morbidity and mortality among vulnerable populations.

          Abstract

          In this data synthesis, Paul Robert Torgerson and colleagues estimate the global and regional disease burden of 11 foodborne parasitic diseases.

          Editors' Summary

          Background

          Foodborne diseases cause a large burden of illness (morbidity) and death (mortality), worldwide. More than 200 diseases can be transmitted to people through the ingestion of food contaminated by microorganisms (viruses, bacteria, and parasites) or with chemicals. Food can become contaminated on the farms where crops and animals are raised, in food processing plants, and during food storage and preparation at home and in restaurants. Food contamination can be caused by pollution of water and soil by human and animal feces and by poor hygiene practices such as not washing one’s hands after using the toilet or before handling food. Many foodborne diseases present with gastrointestinal symptoms (stomach cramps, diarrhea and vomiting) but some also affect other parts of the body and some have serious sequelae (abnormal bodily conditions or diseases arising from a pre-existing disease). For example, the parasitic tapeworm Taenia solium (which is spread by eating undercooked pork) can cause cysticercosis, an infection of tissues by larval cysts that can result in seizures, stroke and death.

          Why Was This Study Done?

          National and international efforts to improve food safety need accurate information on foodborne infections so, in 2007, the World Health Organization (WHO) established the Foodborne Disease Burden Epidemiology Reference Group (FERG) to provide estimates of the global and regional burden of disease attributable to foodborne illnesses. Here, researchers involved in one of FERG’s constituent task forces—the Parasitic Diseases Task Force—combine information from many different sources (a data synthesis) to provide estimates of the regional and global disease burden of ten helminth diseases and toxoplasmosis attributable to contaminated food. Examples of helminths (parasitic worms) include roundworms ( Ascaris lumbricoides; heavy roundworm infections [ascariosis] can cause signs of malnutrition or even intestinal blockages), tapeworms and flukes (liver and lung flukes cause a condition known as trematodosis; frequently transmitted in undercooked fish crustacea or aquatic vegetables). Toxoplasmosis is caused by a parasite found in undercooked meat and in cat feces. If a woman becomes infected during pregnancy, she can pass the parasite onto her unborn child (congenital toxoplasmosis), thereby causing eye problems and sometimes developmental problems and seizures later in life.

          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 topic using predefined criteria), national surveillance programs, and other sources to estimate the number of illnesses, sequelae, and deaths for ten helminth diseases and toxoplasmosis. They also estimated the number of disability adjusted life years (DALYs) globally and regionally for each disease. A DALY is 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. Together, these diseases caused 48.4 million cases of illness, 59,724 deaths, and 8.78 million DALYs in 2010. The researchers estimated that 48% of these cases of parasitic diseases, resulting in 6.64 million DALYs, were transmitted by contaminated food. The commonest foodborne parasitic diseases were Ascaris infection and toxoplasmosis (12.3 million and 10.3 million cases, respectively). Foodborne cysticercosis, trematodosis and toxoplasmosis resulted in the highest disease burdens, and the largest burden of foodborne parasitic disease occurred in the Western Pacific and African regions.

          What Do These Findings Mean?

          The lack of reliable data on the diseases considered in this study for many regions of the world and the use of expert panels to estimate the proportion of each disease that is foodborne may limit the accuracy of these findings. Moreover, this study does not estimate the global burden of every potentially important foodborne parasitic disease. However, these findings, together with those on three foodborne enteric protozoa (single-celled parasites that infect the intestines) included in a related paper, indicate that parasites are frequently transmitted to people through contaminated food and that, although some parasites result in a low burden of disease, foodborne parasites result in significant illness and death that is often borne by relatively small populations in limited geographical areas. This information, together with other estimates on foodborne disease obtained by FERG, should facilitate the development and implementation of effective national and global food safety policies.

          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.1001920.

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          Most cited references30

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          Quantifying the burden of disease: the technical basis for disability-adjusted life years.

          C. Murray (1994)
          Detailed assumptions used in constructing a new indicator of the burden of disease, the disability-adjusted life year (DALY), are presented. Four key social choices in any indicator of the burden of disease are carefully reviewed. First, the advantages and disadvantages of various methods of calculating the duration of life lost due to a death at each age are discussed. DALYs use a standard expected-life lost based on model life-table West Level 26. Second, the value of time lived at different ages is captured in DALYs using an exponential function which reflects the dependence of the young and the elderly on adults. Third, the time lived with a disability is made comparable with the time lost due to premature mortality by defining six classes of disability severity. Assigned to each class is a severity weight between 0 and 1. Finally, a three percent discount rate is used in the calculation of DALYs. The formula for calculating DALYs based on these assumptions is provided.
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            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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              Fascioliasis and other plant-borne trematode zoonoses.

              Fascioliasis and other food-borne trematodiases are included in the list of important helminthiases with a great impact on human development. Six plant-borne trematode species have been found to affect humans: Fasciola hepatica, Fasciola gigantica and Fasciolopsis buski (Fasciolidae), Gastrodiscoides hominis (Gastrodiscidae), Watsonius watsoni and Fischoederius elongatus (Paramphistomidae). Whereas F. hepatica and F. gigantica are hepatic, the other four species are intestinal parasites. The fasciolids and the gastrodiscid cause important zoonoses distributed throughout many countries, while W. watsoni and F. elongatus have been only accidentally detected in humans. Present climate and global changes appear to increasingly affect snail-borne helminthiases, which are strongly dependent on environmental factors. Fascioliasis is a good example of an emerging/re-emerging parasitic disease in many countries as a consequence of many phenomena related to environmental changes as well as man-made modifications. The ability of F. hepatica to spread is related to its capacity to colonise and adapt to new hosts and environments, even at the extreme inhospitality of very high altitude. Moreover, the spread of F. hepatica from its original European range to other continents is related to the geographic expansion of its original European lymnaeid intermediate host species Galba truncatula, the American species Pseudosuccinea columella, and its adaptation to other lymnaeid species authochthonous in the newly colonised areas. Although fasciolopsiasis and gastrodiscoidiasis can be controlled along with other food-borne parasitoses, fasciolopsiasis still remains a public health problem in many endemic areas despite sustained WHO control programmes. Fasciolopsiasis has become a re-emerging infection in recent years and gastrodiscoidiasis, initially supposed to be restricted to Asian countries, is now being reported in African countries.
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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
                : e1001920
                Affiliations
                [1 ]University of Zürich, Zürich, Switzerland
                [2 ]Ghent University, Ghent, Belgium
                [3 ]Université catholique de Louvain, Brussels, Belgium
                [4 ]Institute of Tropical Medicine, Antwerp, Belgium
                [5 ]Ross University School of Veterinary Medicine, St. Kitts, West Indies
                [6 ]National Institute of Health Sciences, Tokyo, Japan
                [7 ]Tehran University of Medical Sciences, Tehran, Iran
                [8 ]Chinese Center for Disease Control and Prevention, Shanghai, People’s Republic of China
                [9 ]University of Liverpool, Liverpool, United Kingdom
                [10 ]International Livestock Research Institute, Nairobi, Kenya
                [11 ]Khon Kaen University, Khon Kaen, Thailand
                [12 ]Hikma Pharmaceuticals, Amman, Jordan
                [13 ]Imperial College, London, United Kingdom
                [14 ]Texas A&M University, College Station, Texas, United States of America
                [15 ]University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma, United States of America
                [16 ]The Australian National University, Canberra, Australia
                [17 ]Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America
                [18 ]National Institute for Public Health and the Environment, Bilthoven, The Netherlands
                [19 ]Utrecht University, Utrecht, The Netherlands
                [20 ]University of Florida, Gainesville, Gainesville, Florida, United States of America
                [21 ]University of Kelaniya, Ragama, Sri Lanka
                Mahidol-Oxford Tropical Medicine Research Unit, THAILAND
                Author notes

                PRT, BD, NP, NS, ALW, FK, MBR, XNZ, EMF, BS, NG, MDK, FJA, AH & NdS serve as members of the World Health Organization advisory body—the Foodborne Disease Epidemiology Reference Group—without remuneration. The authors declare no further competing interests.

                Conceived and designed the experiments: PRT NS ALW FK MBR XNZ AMF BS NG AH NS EMF. Performed the experiments: PRT NP NS TF CMB HC MDK FJA. Analyzed the data: PRT BD TF CMB HC MDK FJA. Contributed reagents/materials/analysis tools: BD. Wrote the first draft of the manuscript: PRT. Contributed to the writing of the manuscript: PRT BD NP NS ALW TF MDK FJA AH EMF. Agree with the manuscript’s results and conclusions: PRT BD NP NS ALW FK MBR XNZ EMF BS NG TF CMB HC MDK FJA AH NS. Designed software used in analysis: BD. All authors have read, and confirm that they meet, ICMJE criteria for authorship.

                Article
                PMEDICINE-D-15-01157
                10.1371/journal.pmed.1001920
                4668834
                26633705
                a7e9d062-c52c-43e6-a89c-c9936ec7aa32

                Copyright: ©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
                : 16 April 2015
                : 2 November 2015
                Page count
                Figures: 4, Tables: 3, Pages: 22
                Funding
                This study was commissioned and paid for by the World Health Organization (WHO) ( http://www.who.int). Copyright in the original work on which this article is based belongs to WHO. The authors have been given permission to publish this article.
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                Medicine
                Medicine

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