World Health Organization estimates of the global and regional disease burden of four foodborne chemical toxins, 2010: a data synthesis

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Abstract

Background

Chemical exposures have been associated with a variety of health effects; however, little is known about the global disease burden from foodborne chemicals. Food can be a major pathway for the general population’s exposure to chemicals, and for some chemicals, it accounts for almost 100% of exposure.

Methods and Findings

Groups of foodborne chemicals, both natural and anthropogenic, were evaluated for their ability to contribute to the burden of disease. The results of the analyses on four chemicals are presented here - cyanide in cassava, peanut allergen, aflatoxin, and dioxin. Systematic reviews of the literature were conducted to develop age- and sex-specific disease incidence and mortality estimates due to these chemicals. From these estimates, the numbers of cases, deaths and disability adjusted life years (DALYs) were calculated. For these four chemicals combined, the total number of illnesses, deaths, and DALYs in 2010 is estimated to be 339,000 (95% uncertainty interval [UI]: 186,000-1,239,000); 20,000 (95% UI: 8,000-52,000); and 1,012,000 (95% UI: 562,000-2,822,000), respectively. Both cyanide in cassava and aflatoxin are associated with diseases with high case-fatality ratios. Virtually all human exposure to these four chemicals is through the food supply.

Conclusion

Chemicals in the food supply, as evidenced by the results for only four chemicals, can have a significant impact on the global burden of disease. The case-fatality rates for these four chemicals range from low (e.g., peanut allergen) to extremely high (aflatoxin and liver cancer). The effects associated with these four chemicals are neurologic (cyanide in cassava), cancer (aflatoxin), allergic response (peanut allergen), endocrine (dioxin), and reproductive (dioxin).

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Most cited references 38

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The 2005 World Health Organization reevaluation of human and Mammalian toxic equivalency factors for dioxins and dioxin-like compounds.

Martin van den Berg, Linda S. Birnbaum, Michael H. Denison … (2006)

In June 2005, a World Health Organization (WHO)-International Programme on Chemical Safety expert meeting was held in Geneva during which the toxic equivalency factors (TEFs) for dioxin-like compounds, including some polychlorinated biphenyls (PCBs), were reevaluated. For this reevaluation process, the refined TEF database recently published by Haws et al. (2006, Toxicol. Sci. 89, 4-30) was used as a starting point. Decisions about a TEF value were made based on a combination of unweighted relative effect potency (REP) distributions from this database, expert judgment, and point estimates. Previous TEFs were assigned in increments of 0.01, 0.05, 0.1, etc., but for this reevaluation, it was decided to use half order of magnitude increments on a logarithmic scale of 0.03, 0.1, 0.3, etc. Changes were decided by the expert panel for 2,3,4,7,8-pentachlorodibenzofuran (PeCDF) (TEF = 0.3), 1,2,3,7,8-pentachlorodibenzofuran (PeCDF) (TEF = 0.03), octachlorodibenzo-p-dioxin and octachlorodibenzofuran (TEFs = 0.0003), 3,4,4',5-tetrachlorbiphenyl (PCB 81) (TEF = 0.0003), 3,3',4,4',5,5'-hexachlorobiphenyl (PCB 169) (TEF = 0.03), and a single TEF value (0.00003) for all relevant mono-ortho-substituted PCBs. Additivity, an important prerequisite of the TEF concept was again confirmed by results from recent in vivo mixture studies. Some experimental evidence shows that non-dioxin-like aryl hydrocarbon receptor agonists/antagonists are able to impact the overall toxic potency of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) and related compounds, and this needs to be investigated further. Certain individual and groups of compounds were identified for possible future inclusion in the TEF concept, including 3,4,4'-TCB (PCB 37), polybrominated dibenzo-p-dioxins and dibenzofurans, mixed polyhalogenated dibenzo-p-dioxins and dibenzofurans, polyhalogenated naphthalenes, and polybrominated biphenyls. Concern was expressed about direct application of the TEF/total toxic equivalency (TEQ) approach to abiotic matrices, such as soil, sediment, etc., for direct application in human risk assessment. This is problematic as the present TEF scheme and TEQ methodology are primarily intended for estimating exposure and risks via oral ingestion (e.g., by dietary intake). A number of future approaches to determine alternative or additional TEFs were also identified. These included the use of a probabilistic methodology to determine TEFs that better describe the associated levels of uncertainty and "systemic" TEFs for blood and adipose tissue and TEQ for body burden.

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A new method for determining allowable daily intakes.

K S Crump (1984)

The usual method for establishing allowable daily intake (ADI) for a chemical involves determining a no-observed-effect level (NOEL) and applying a safety factor. Even though this method has been used for many years, there appear to be no general guidelines or rules for defining a NOEL. The determination of a NOEL is particularly uncertain for lesions which occur naturally in untreated animals. NOELs also have shortcomings in that smaller experiments tend to give larger values (this should be reversed because larger experiments can provide greater evidence of safety) and that the steepness of the dose response in the dose range where effects occur plays little or no role in the determination of a NOEL. This paper proposes and illustrates the use of a "benchmark dose" (BD) as an alternative to a NOEL. A BD is a statistical lower confidence limit to a dose producing some predetermined increase in response rate such as 0.01 or 0.1. The BD is calculated using a mathematical dose-response model. This approach makes appropriate use of sample size and the shape of the dose-response curve. The BD normally will not depend strongly upon the mathematical model used because the method does not involve extrapolation far below the experimental range. Thus the method sidesteps much of the model dependency often associated with extrapolation of carcinogenicity data to low doses. The method can be applied to either "quantal" data in which only the presence or absence of an effect is recorded, or "continuous" data in which the severity of the effect is also noted.

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Serum TSH and total T4 in the United States population and their association with participant characteristics: National Health and Nutrition Examination Survey (NHANES 1999-2002).

Yutaka Aoki, Kathryn Mahaffey, T Belin … (2007)

Describe thyrotropin (TSH) and thyroxine (T4) levels in the U.S. population and their association with selected participant characteristics. Secondary analysis of data from the National Health and Nutrition Examination Survey (NHANES) collected from 4392 participants, reflecting 222 million individuals, during 1999-2002. Hypothyroidism prevalence (TSH > 4.5 mIU/L) in the general population was 3.7%, and hyperthyroidism prevalence (TSH < 0.1 mIU/L) was 0.5%. Among women of reproductive age (12-49 years), hypothyroidism prevalence was 3.1%. Individuals aged 80 years and older had five times greater odds for hypothyroidism compared to 12- to 49-year-olds (adjusted odds ratio [OR] = 5.0, p = 0.0002). ORs were adjusted for sex, race, annual income, pregnancy status, and usage of thyroid-related medications (levothyroxine/thyroid, estrogen, androgen, lithium, and amiodarone). Compared to non-Hispanic whites, non-Hispanic blacks had a lower risk for hypothyroidism (OR = 0.46, p = 0.04) and a higher risk for hyperthyroidism (OR = 3.18, p = 0.0005), while Mexican Americans had the same risk as non-Hispanic whites for hypothyroidism, but a higher risk for hyperthyroidism (OR = 1.98, p = 0.04). Among those taking levothyroxine or desiccated thyroid, the adjusted risk for either hypothyroidism (OR = 4.0, p = 0.0001) or hyperthyroidism (OR = 11.4, p = 4 x 10(-9)) was elevated. Associations with known factors such as age, race, and sex were confirmed using this data set. Understanding the prevalence of abnormal thyroid tests among reproductive-aged women informs decisions about screening in this population. The finding that individuals on thyroid hormone replacement medication often remain hypothyroid or become hyperthyroid underscores the importance of monitoring.

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Author and article information

Journal

Journal ID (nlm-ta): F1000Res

Journal ID (iso-abbrev): F1000Res

Journal ID (pmc): F1000Research

Title: F1000Research

Publisher: F1000Research (London, UK )

ISSN (Electronic): 2046-1402

Publication date (Electronic): 3 December 2015

Publication date Collection: 2015

Volume: 4

Electronic Location Identifier: 1393

Affiliations

[1 ]Gibb Epidemiology Consulting LLC, Arlington, VA, USA

[2 ]Department of Virology, Parasitology and Immunology, Ghent University, Merelbeke, Belgium

[3 ]Institute of Health and Society (IRSS), Université catholique de Louvain, Brussels, Belgium

[4 ]Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium

[5 ]Exponent, Center for Chemical Regulation and Food Safety, Washington, DC, USA

[6 ]Department of Food Science and Human Nutrition, Michigan State University, East Lansing, MI, USA

[7 ]Department of Agricultural, Food, and Resource Economics, Michigan State University, East Lansing, MI, USA

[8 ]National Institute for Public Health and the Environment (RIVM), Bilthoven, Netherlands

[9 ]Faculdade de Medicina, Universidade Eduardo Mondlane, Maputo, Mozambique

[10 ]Department of Food Safety and Zoonoses, World Health Organization, Geneva, Switzerland

[11 ]CSIRO Food and Nutrition Flagship, North Ryde, Australia

[12 ]Food Data Analysis Section, Food Standards Australia New Zealand, Canberra, Australia

[13 ]Department of Food Technology, University of Ibadan, Ibadan, Nigeria

[14 ]Environmental Health Services, British Columbia Centre for Disease Control, Vancouver, BC, Canada

[15 ]INTERTEK, Oak Brook, IL, USA

[16 ]Emerging Pathogens Institute and Animal Sciences Department, University of Florida, Gainesville, FL, USA

[17 ]Institute for Risk Assessment Sciences, Utrecht University, Utrecht, Netherlands

[18 ]Boston Children’s Hospital, Harvard Medical School, Boston, MA, USA

[1 ]Department of Health Policy and Management, Johns Hopkins University Bloomberg School of Public Health, Baltimore, MD, USA

[1 ]Department of Environmental and Occupational Health, George Washington University, Milken Institute School of Public Health, Washington, D.C, USA

[1 ]Division of Allergy, Children’s Hospital of Pennsylvania, Philadelphia, PA, USA

Gibb Epidemiology Consulting LLC, USA

Author notes

[a ] herman.gibb@ 123456gibbepi.com

Conceived and designed the experiments: HG, PMB, FW, JE, JC, MZ, PV, JIP, JB, GA, RA, YL, BB, HL, ML, AH, DB, EB.

Performed the experiments: FW, JE, JC, MZ, YL, BB, HL, MM, EB.

Analyzed the data: BD, FW, JE, JC, MZ, YL, BB, HL, MM, EB.

Wrote the first draft of the manuscript: HG.

Contributed to the writing of the manuscript: HG, AH, BD, DB, PMB, MZ, BB, JP, JB.

ICMJE criteria for authorship read and met: HG, BD, PMB, FW, JE, JC, MZ, PV, JIP, JB, GA, RA, YL, BB, HL, ML, AH, DB, EB.

Agree with manuscript results and conclusions: HG, BD, PMB, FW, JE, JC, MZ, PV, JIP, JB, GA, RA, YL, BB, HL, ML, AH, DB, EB.

Competing interests: HJG, BD, MPB, AHH, JB, PV, JIP, GA, RA, and DCB serve as members of the World Health Organization advisory body—the Foodborne Disease Burden Epidemiology Reference Group - without remuneration. The authors declare no competing interests.

Competing interests: No competing interests were disclosed.

Competing interests: There are no competing interests.

Article

DOI: 10.12688/f1000research.7340.1

PMC ID: 4755404

PubMed ID: 26918123

SO-VID: 447937ae-c163-4e70-83b4-c5e5ee805469

License:

This is an open access article distributed under the terms of the Creative Commons Attribution IGO Licence.

History

Date accepted : 19 November 2015

Funding

Funded by: World Health Organization

Funded by: National Institute for Public Health and the Environment, Bilthoven

Funded by: Netherlands and the Ministry of Public Health, Welfare, and Sports, the Hague

This study was commissioned by the World Health Organization (WHO). Funding for the work on aflatoxin and cyanide in cassava was provided by the WHO. The work on peanut allergy and dioxin was done through in-kind support provided by the National Institute for Public Health and the Environment, Bilthoven, the Netherlands and the Ministry of Public Health, Welfare, and Sports, the Hague. Copyright in the original work on which this article is based belongs to WHO. The authors have been given permission to publish this article. The author(s) alone are responsible for the views expressed in this publication and they do not necessarily represent the views, decisions or policies of the World Health Organization.

World Health Organization estimates of the global and regional disease burden of four foodborne chemical toxins, 2010: a data synthesis

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Most cited references 38

The 2005 World Health Organization reevaluation of human and Mammalian toxic equivalency factors for dioxins and dioxin-like compounds.

A new method for determining allowable daily intakes.

Serum TSH and total T4 in the United States population and their association with participant characteristics: National Health and Nutrition Examination Survey (NHANES 1999-2002).

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