{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,12]],"date-time":"2025-10-12T03:58:07Z","timestamp":1760241487577,"version":"build-2065373602"},"reference-count":66,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2018,3,23]],"date-time":"2018-03-23T00:00:00Z","timestamp":1521763200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Nutrients"],"abstract":"<jats:p>Multiple drivers of the double burden of malnutrition (DBM) include a rapid shift from predominantly plant-based diets to energy-dense foods based on meats, milk, animal fats and vegetable oils. The shift to overweight and obesity is driven by increased exposure to mass media, urbanization, technological advances in food processing, rising income and increased population density associated with increased access to cheap foods. At the same time, undernutrition persists mainly due to food insecurity and lack of access to safe water, sanitation and adequate health care. All known nutrition interventions result in only one third reduction in stunting. Little consideration has been given to hazardous exposure to endocrine disrupting chemicals (EDCs) and microbial toxins as major components of the malnutrition-causal framework. These hazards include microbial toxins, for example, mycotoxins, and environmental pollutants such as persistent organic pollutants (POPs), some of which are known to disrupt the endocrine system. These hazards sit at the cross road of undernutrition and overweight and obesity since the exposure cuts across the critical window of opportunity (the first 1000 days). In this review, we update on the role of food and environmental contaminants, especially EDCs and aflatoxins, in child growth and on the implications for metabolic dysfunction and disease risk in later life, and discuss potential applications of nuclear and isotopic techniques to elucidate the underlying biological mechanisms, outcome indicators, as well as occurrence levels.<\/jats:p>","DOI":"10.3390\/nu10040401","type":"journal-article","created":{"date-parts":[[2018,3,23]],"date-time":"2018-03-23T12:28:19Z","timestamp":1521808099000},"page":"401","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Elucidating Adverse Nutritional Implications of Exposure to Endocrine-Disrupting Chemicals and Mycotoxins through Stable Isotope Techniques"],"prefix":"10.3390","volume":"10","author":[{"given":"Victor","family":"Owino","sequence":"first","affiliation":[{"name":"Nutrition and Health Related Environmental Studies Section, Division of Health, International Atomic Energy Agency, Vienna International Centre P.O. Box 100, A-1400 Vienna, Austria"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Carolin","family":"Cornelius","sequence":"additional","affiliation":[{"name":"Nutrition and Health Related Environmental Studies Section, Division of Health, International Atomic Energy Agency, Vienna International Centre P.O. Box 100, A-1400 Vienna, Austria"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Cornelia","family":"Loechl","sequence":"additional","affiliation":[{"name":"Nutrition and Health Related Environmental Studies Section, Division of Health, International Atomic Energy Agency, Vienna International Centre P.O. Box 100, A-1400 Vienna, Austria"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2018,3,23]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"International food policy research institute (2016). From promise to impact: Ending malnutrition by 2030. Global Nutrition Report 2016, International Food Policy Research Institute.","DOI":"10.2499\/9780896295841"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1170","DOI":"10.3945\/ajcn.113.064584","article-title":"Adult consequences of growth failure in early childhood","volume":"98","author":"Hoddinott","year":"2013","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_3","unstructured":"(2017, November 23). Work Programme of the United Nations Decade of Action on Nutrition (2016\u20132025). Available online: http:\/\/www.who.int\/nutrition\/decade-of-action\/workprogramme-2016to2025\/en\/."},{"key":"ref_4","unstructured":"Kennedy, G., Nantel, G., and Shetty, P. (2006). Assessment of the Double Burden of Malnutrition in Six Case Study Countries, FAO. FAO Food and Nutrients Paper."},{"key":"ref_5","unstructured":"(2018, March 16). The World Bank. Available online: https:\/\/datahelpdesk.worldbank.org\/knowledgebase\/articles\/906519-world-bank-country-and-lending-groups."},{"key":"ref_6","unstructured":"(2017, December 23). Trends towards Overweight in Lower and Middle-Income Countries: Some Causes and Economic Policy Options. Available online: http:\/\/www.fao.org\/docrep\/009\/a0442e\/a0442e0x.htm."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1016\/S0140-6736(07)61693-6","article-title":"Maternal and child undernutrition 3\u2013what works? Interventions for maternal and child undernutrition and survival","volume":"371","author":"Bhutta","year":"2008","journal-title":"Lancet"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1177\/156482651303400308","article-title":"Implications of acquired environmental enteric dysfunction for growth and stunting in infants and children living in low- and middle-income countries","volume":"34","author":"Keusch","year":"2013","journal-title":"Food Nutr. Bull."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1111\/mcn.12220","article-title":"Preventing environmental enteric dysfunction through improved water, sanitation and hygiene: An opportunity for stunting reduction in developing countries","volume":"12","author":"Mbuya","year":"2016","journal-title":"Matern. Child Nutr."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Owino, V., Ahmed, T., Freemark, M., Kelly, P., Loy, A., Manary, M., and Loechl, C. (2016). Environmental enteric dysfunction and growth failure\/stunting in global child health. Pediatrics, 138.","DOI":"10.1542\/peds.2016-0641"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"952","DOI":"10.1001\/archpediatrics.2012.241","article-title":"Exposure to environmental endocrine disruptors and child development","volume":"166","author":"Meeker","year":"2012","journal-title":"Arch. Pediatr. Adolesc. Med."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1210\/er.2009-0002","article-title":"Endocrine-disrupting chemicals: An endocrine society scientific statement","volume":"30","author":"Bourguignon","year":"2009","journal-title":"Endocr. Rev."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"4097","DOI":"10.1210\/en.2012-1422","article-title":"Endocrine-disrupting chemicals and public health protection: A statement of principles from The Endocrine Society","volume":"153","author":"Zoeller","year":"2012","journal-title":"Endocrinology"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1334","DOI":"10.1289\/ehp.6954","article-title":"Postweaning exposure to aflatoxin results in impaired child growth: A longitudinal study in Benin, west Africa","volume":"112","author":"Gong","year":"2004","journal-title":"Environ. Health Perspect."},{"key":"ref_15","first-page":"14","article-title":"Aflatoxin exposure and associated human health effects","volume":"4","author":"Gong","year":"2016","journal-title":"Food Saf. Off. J. Food Saf. Comm. Jpn."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1016\/j.envint.2013.03.008","article-title":"Associations between PFOA, PFOS and changes in the expression of genes involved in cholesterol metabolism in humans","volume":"57\u201358","author":"Fletcher","year":"2013","journal-title":"Environ. Int."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/j.aogh.2016.01.008","article-title":"Effects of environmental exposures on fetal and childhood growth trajectories","volume":"82","author":"Zheng","year":"2016","journal-title":"Ann. Glob. Health"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"849","DOI":"10.1007\/s00125-005-1724-4","article-title":"Dynamic change in adiposity from fetal to postnatal life is involved in the metabolic syndrome associated with reduced fetal growth","volume":"48","author":"Jaquet","year":"2005","journal-title":"Diabetologia"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"538","DOI":"10.1203\/00006450-199810000-00012","article-title":"Effects of environmental exposure to polychlorinated biphenyls and dioxins on birth size and growth in Dutch children","volume":"44","author":"Patandin","year":"1998","journal-title":"Pediatr. Res."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1677","DOI":"10.1289\/ehp.10506","article-title":"Perfluorinated chemicals and fetal growth: A study within the Danish National Birth Cohort","volume":"115","author":"Fei","year":"2007","journal-title":"Environ. Health Perspect."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"740","DOI":"10.3109\/10408444.2011.575766","article-title":"Aflatoxins and growth impairment: A review","volume":"41","author":"Khlangwiset","year":"2011","journal-title":"Crit. Rev. Toxicol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1289\/ehp.5753","article-title":"Modification of immune function through exposure to dietary aflatoxin in Gambian children","volume":"111","author":"Turner","year":"2003","journal-title":"Environ. Health Perspect."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"612","DOI":"10.1016\/j.tem.2017.05.001","article-title":"Gut microbiota, endocrine-disrupting chemicals, and the diabetes epidemic","volume":"28","author":"Velmurugan","year":"2017","journal-title":"Trends Endocrinol. Metab."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"396","DOI":"10.3390\/toxins5020396","article-title":"Modulation of intestinal functions following mycotoxin ingestion: Meta-analysis of published experiments in animals","volume":"5","author":"Grenier","year":"2013","journal-title":"Toxins"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Petrakis, D., Vassilopoulou, L., Mamoulakis, C., Psycharakis, C., Anifantaki, A., Sifakis, S., Docea, A.O., Tsiaoussis, J., Makrigiannakis, A., and Tsatsakis, A.M. (2017). Endocrine disruptors leading to obesity and related diseases. Int. J. Environ. Res. Public Health, 14.","DOI":"10.3390\/ijerph14101282"},{"key":"ref_26","unstructured":"(2017, November 23). State of the Science of Endocrine Disrupting Chemicals\u20132012. Available online: http:\/\/www.who.int\/ceh\/publications\/endocrine\/en\/."},{"key":"ref_27","unstructured":"Lichtfouse, E., Schwarzbauer, J., and Robert, D. (2012). Organic pollutants as endocrine disruptors: Organometallics, PAHs, organochlorine, organophosphate and carbamate insecticides, phthalates, dioxins, phytoestrogens, alkyl phenols and bisphenol A. Environmental Chemistry for a Sustainable World, Springer."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1097\/MED.0b013e32835b7ee6","article-title":"The influence of endocrine disruptors on growth and development of children","volume":"20","author":"DiVall","year":"2013","journal-title":"Curr. Opin. Endocrinol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1939S","DOI":"10.3945\/ajcn.110.001057","article-title":"Developmental exposure to endocrine-disrupting chemicals programs for reproductive tract alterations and obesity later in life","volume":"94","author":"Newbold","year":"2011","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_30","unstructured":"Klaassen, C. (2013). Developmental Toxicology. Casarett & Doull\u2019s Toxicology: The Basic Science of Poisons, McGraw-Hill Education. [8th ed.]."},{"key":"ref_31","unstructured":"World Health Organization (WHO) (2017, September 05). Endocrine Disorders and Children, Children\u2019s Health and the Environment. Available online: http:\/\/www.portal.pmnch.org\/ceh\/capacity\/endocrine.pdf."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"912","DOI":"10.1080\/10934529.2013.762734","article-title":"Association between precocious puberty and some endocrine disruptors in human plasma","volume":"48","author":"Yum","year":"2013","journal-title":"J. Environ. Sci. Health A"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1093\/humupd\/dmh012","article-title":"Precocious puberty and statural growth","volume":"10","author":"Carel","year":"2004","journal-title":"Hum. Reprod. Update"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1785","DOI":"10.1289\/EHP208","article-title":"Occupational exposure to endocrine-disrupting chemicals and birth weight and length of gestation: A European meta-analysis","volume":"124","author":"Birks","year":"2016","journal-title":"Environ. Health Perspect."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"59","DOI":"10.4236\/ojemd.2017.71007","article-title":"Endocrine disruptors and fetal programming","volume":"7","author":"Lucchese","year":"2017","journal-title":"OJEMD"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1933","DOI":"10.3945\/ajcn.110.001669","article-title":"The obelix project: Early life exposure to endocrine disruptors and obesity","volume":"94","author":"Legler","year":"2011","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"191","DOI":"10.5114\/aoms.2013.33181","article-title":"Biochemistry of adipose tissue: An endocrine organ","volume":"9","author":"Coelho","year":"2013","journal-title":"Arch. Med. Sci."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"S53","DOI":"10.1038\/ijo.2008.207","article-title":"Interference of pollutants with PPARs: Endocrine disruption meets metabolism","volume":"32","author":"Feige","year":"2008","journal-title":"Int. J. Obes."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/j.mce.2009.02.018","article-title":"Endocrine disrupters as obesogens","volume":"304","author":"Grun","year":"2009","journal-title":"Mol. Cell. Endocrinol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"324","DOI":"10.1111\/j.1365-2605.2009.01035.x","article-title":"Association of endocrine disruptors and obesity: Perspectives from epidemiological studies","volume":"33","author":"Hatch","year":"2010","journal-title":"Int. J. Androl."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"5","DOI":"10.3945\/ajcn.113.066720","article-title":"Association between prenatal polychlorinated biphenyl exposure and obesity development at ages 5 and 7 y: A prospective cohort study of 656 children from the Faroe Islands","volume":"99","author":"Heitmann","year":"2014","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"407","DOI":"10.1016\/j.envres.2015.07.009","article-title":"Prenatal exposure to persistent organochlorine pollutants is associated with high insulin levels in 5-year-old girls","volume":"142","author":"Heitmann","year":"2015","journal-title":"Environ. Res."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1017\/S0029665100000288","article-title":"Interactions of perturbations in intrauterine growth and growth during childhood on the risk of adult-onset disease","volume":"59","author":"Yajnik","year":"2000","journal-title":"Proc. Nutr. Soc."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"184","DOI":"10.1016\/j.fct.2014.09.016","article-title":"Aflatoxin exposure during the first 1000 days of life in rural south Asia assessed by aflatoxin B1-lysine albumin biomarkers","volume":"74","author":"Groopman","year":"2014","journal-title":"Food Chem. Toxicol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1106","DOI":"10.1093\/ajcn\/80.5.1106","article-title":"Human aflatoxicosis in developing countries: A review of toxicology, exposure, potential health consequences, and interventions","volume":"80","author":"Williams","year":"2004","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1016\/j.ijfoodmicro.2005.03.004","article-title":"Dietary exposure to aflatoxin from maize and groundnut in young children from Benin and Togo, West Africa","volume":"15","author":"Egal","year":"2005","journal-title":"Int. J. Food Microbiol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1794","DOI":"10.1289\/ehp.1003044","article-title":"Comprehensive assessment of maize aflatoxin levels in eastern Kenya, 2005\u20132007","volume":"119","author":"Daniel","year":"2011","journal-title":"Environ. Health Perspect."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Modupeade, C., Adetunji, A.O., and Chibundu, E.N. (2017). Risk Assessment of Mycotoxins in stored maize grains consumed by infants and young children in Nigeria. Children, 4.","DOI":"10.3390\/children4070058"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1016\/S0015-6264(73)80331-1","article-title":"Excretion and metabolism of orally administered aflatoxin B1 by rhesus monkeys","volume":"11","author":"Dalezios","year":"1973","journal-title":"Food Cosmet. Toxicol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"556","DOI":"10.1093\/ije\/dyg109","article-title":"Determinants of aflatoxin exposure in young children from Benin and Togo, west Africa: The critical role of weaning","volume":"32","author":"Gong","year":"2003","journal-title":"Int. J. Epidemiol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1080\/1354750X.2017.1285960","article-title":"Comparison of urinary aflatoxin M1 and aflatoxin albumin adducts as biomarkers for assessing aflatoxin exposure in Tanzanian children","volume":"23","author":"Chen","year":"2018","journal-title":"Biomarkers"},{"key":"ref_52","first-page":"273","article-title":"Aflatoxins in the livers of children with kwashiorkor in Ghana","volume":"38","author":"Apeagyei","year":"1986","journal-title":"Trop. Geogr. Med."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1038\/pr.2015.84","article-title":"Dietary aflatoxin-induced stunting in a novel rat model: Evidence for toxin-induced liver injury and hepatic growth hormone resistance","volume":"78","author":"Knipstein","year":"2015","journal-title":"Pediatr. Res."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"398","DOI":"10.1182\/blood.V98.2.398","article-title":"Impaired progenitor cell function in HIV-negative infants of HIV-positive mothers results in decreased thymic output and low CD4 counts","volume":"98","author":"Nielsen","year":"2001","journal-title":"Blood"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"S37","DOI":"10.1097\/00126334-200010001-00006","article-title":"Growth failure in children with HIV infection","volume":"25","author":"Arpadi","year":"2000","journal-title":"J. Acquir. Immune Defic. Syndr."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1017\/S0029665117000295","article-title":"Using stable isotope techniques in nutrition assessments and tracking of global targets post\u20132015","volume":"76","author":"Owino","year":"2017","journal-title":"Proc. Nutr. Soc."},{"key":"ref_57","first-page":"101","article-title":"Availability of arsenic in human milk in women and its correlation with arsenic in urine of breastfed children living in arsenic contaminated areas in Bangladesh","volume":"13","author":"Islam","year":"2014","journal-title":"Environ. Health A Glob."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"617","DOI":"10.1007\/s00216-007-1717-x","article-title":"Stable isotope dilution assays in mycotoxin analysis","volume":"390","author":"Rychlik","year":"2008","journal-title":"Anal. Bioanal. Chem."},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"Rochat, T.J., Houle, B., Stein, A., Coovadia, H., Coutsoudis, A., Desmond, C., Newell, M.L., and Bland, R.M. (2016). Exclusive breastfeeding and cognition, executive function, and behavioural disorders in primary school-aged children in rural South Africa: A cohort analysis. PLoS Med., 13.","DOI":"10.1371\/journal.pmed.1002044"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"557","DOI":"10.1210\/er.2013-1084","article-title":"Chlorinated persistent organic pollutants, obesity, and type 2 diabetes","volume":"35","author":"Lee","year":"2014","journal-title":"Endocr. Rev."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"336","DOI":"10.1016\/j.scitotenv.2013.01.024","article-title":"Individual breast milk consumption and exposure to PCBs and PCDD\/Fs in Hungarian infants: A time-course analysis of the first three months of lactation","volume":"449","author":"Vigh","year":"2013","journal-title":"Sci. Total Environ."},{"key":"ref_62","unstructured":"International Atomic Energy Agency (IAEA) (2010). Stable Isotope Technique to Assess Intake of Human Milk in Breastfed Infants, IAEA."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1038\/sj.ijo.802219","article-title":"Neonatal anthropometry: The thin-fat Indian baby. The Pune maternal nutrition study","volume":"27","author":"Yajnik","year":"2003","journal-title":"Int. J. Obes."},{"key":"ref_64","unstructured":"International Atomic Energy Agency (IAEA) (2011). Introduction to Body Composition Assessment Using the Deuterium Dilution Technique with Analysis of Saliva Samples by Fourier Transform Infrared Spectrometry, IAEA."},{"key":"ref_65","unstructured":"International Atomic Energy Agency (IAEA) (2011). Dual Energy X ray Absorptiometry for Bone Mineral Density and Body Composition Assessment, IAEA."},{"key":"ref_66","unstructured":"International Atomic Energy Agency (IAEA) (2009). Assessment of Body Composition and Total Energy Expenditure in Humans Using Stable Isotope Techniques, IAEA."}],"container-title":["Nutrients"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-6643\/10\/4\/401\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T14:58:16Z","timestamp":1760194696000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-6643\/10\/4\/401"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,3,23]]},"references-count":66,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2018,4]]}},"alternative-id":["nu10040401"],"URL":"https:\/\/doi.org\/10.3390\/nu10040401","relation":{},"ISSN":["2072-6643"],"issn-type":[{"type":"electronic","value":"2072-6643"}],"subject":[],"published":{"date-parts":[[2018,3,23]]}}}