{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,22]],"date-time":"2026-09-22T11:48:19Z","timestamp":1790077699361,"version":"4.0.1"},"reference-count":65,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2019,9,1]],"date-time":"2019-09-01T00:00:00Z","timestamp":1567296000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100006488","name":"Institut National de la Recherche Agronomique","doi-asserted-by":"publisher","award":["34000653"],"award-info":[{"award-number":["34000653"]}],"id":[{"id":"10.13039\/501100006488","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Nutrients"],"abstract":"<jats:p>Dietary iron deficiency (ID) is the first nutritional deficiency in the world, in terms of disability adjusted life years (DALY). This nutritional deficiency may lead to anemia, especially among children, adolescents, and adult women. The aim of this study was to build an original probabilistic model to quantitatively assess the ID, the iron deficiency anemia (IDA) and the subsequent health burden in France expressed in DALY, per age class and gender. The model considered the distribution of absorbed iron intake, the iron requirement distribution established by the European Food Safety Authority and the iron status in France. Uncertainty due to lack of data and variability due to biological diversity were taken into account and separated using a second-order Monte Carlo procedure. A total of 1290 (95% CI = 1230\u20131350) IDA cases corresponding to 16 (95% CI = 11\u201320) DALY were estimated per 100,000 individuals per year. The major contributors to IDA burden were menstruating females aged from 25 to 44 years old. Then, a consumption scenario was built with ground beef as intake, an increase in red meat consumption to 100 g\/d would not eliminate entirely the IDA burden. The quantitative methodology applied here for France could be reused for other populations.<\/jats:p>","DOI":"10.3390\/nu11092045","type":"journal-article","created":{"date-parts":[[2019,9,2]],"date-time":"2019-09-02T03:16:12Z","timestamp":1567394172000},"page":"2045","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":12,"title":["Estimation of the Burden of Iron Deficiency Anemia in France from Iron Intake: Methodological Approach"],"prefix":"10.3390","volume":"11","author":[{"given":"Juliana","family":"De Oliveira Mota","sequence":"first","affiliation":[{"name":"Secalim, INRA, Oniris, Universit\u00e9 Bretagne Loire, 44307 Nantes, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Patrick","family":"Tounian","sequence":"additional","affiliation":[{"name":"Service de nutrition et gastroent\u00e9rologie p\u00e9diatriques, h\u00f4pital Trousseau, Sorbonne Universit\u00e9, AP\u2013HP, 75012 Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sandrine","family":"Guillou","sequence":"additional","affiliation":[{"name":"Secalim, INRA, Oniris, Universit\u00e9 Bretagne Loire, 44307 Nantes, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fabrice","family":"Pierre","sequence":"additional","affiliation":[{"name":"INRA, ToxAlim (Research Centre in Food Toxicology), Universit\u00e9 de Toulouse, INRA, ENVT, INP-Purpan, UPS, 31027 Toulouse, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6751-4426","authenticated-orcid":false,"given":"Jeanne-Marie","family":"Membr\u00e9","sequence":"additional","affiliation":[{"name":"Secalim, INRA, Oniris, Universit\u00e9 Bretagne Loire, 44307 Nantes, France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2019,9,1]]},"reference":[{"key":"ref_1","unstructured":"WHO\/CDC (2004). Assessing the Iron Status of Populations: Including Literature Reviews, WHO\/CDC."},{"key":"ref_2","unstructured":"WHO\/UNICEF\/UNU (2001). Iron Deficiency Anaemia: Assessment, Prevention and Control, a Guide for Programme Managers, World Health Organization."},{"key":"ref_3","first-page":"2087","article-title":"Iron deficiency and cognitive functions","volume":"10","year":"2014","journal-title":"Neuropsychiatr. Dis. Treat."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1016\/j.hoc.2015.11.002","article-title":"The global burden of anemia","volume":"30","author":"Kassebaum","year":"2016","journal-title":"Hematol. Oncol. Clin. N. Am."},{"key":"ref_5","unstructured":"WHO\/CDC (2008). Worldwide Prevalence of Anaemia 1993\u20132005: WHO Global Database on Anaemia, WHO\/CDC."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"5S2","DOI":"10.1016\/S0929-693X(17)24002-0","article-title":"Causes des d\u00e9ficits en fer chez l\u2019enfant","volume":"24","author":"Olives","year":"2017","journal-title":"Arch. P\u00e9diatrie"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1155\/2018\/9394060","article-title":"Limitations of Serum Ferritin in Diagnosing Iron Deficiency in Inflammatory Conditions","volume":"2018","author":"Dignass","year":"2018","journal-title":"Int. J. Chronic Dis."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1082","DOI":"10.1002\/ccr3.1529","article-title":"Iron deficiency without anemia\u2014A clinical challenge","volume":"6","author":"Soppi","year":"2018","journal-title":"Clin. Case Rep."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"S99","DOI":"10.1177\/15648265030244S106","article-title":"Iron deficiency: Global prevalence and consequences","volume":"24","author":"Stoltzfus","year":"2003","journal-title":"Food Nutr. Bull."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"5s23","DOI":"10.1016\/S0929-693X(17)24006-8","article-title":"Iron in nutrition","volume":"24","author":"Tounian","year":"2017","journal-title":"Arch. Pediatr."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1016\/j.meatsci.2016.09.012","article-title":"Iron in red meat\u2013friend or foe","volume":"123","author":"Czerwonka","year":"2017","journal-title":"Meat Sci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"722","DOI":"10.1097\/MPG.0b013e3182a80c42","article-title":"Anemia and iron deficiency in children: Association with red meat and poultry consumption","volume":"57","author":"Moshe","year":"2013","journal-title":"J. Pediatr. Gastroenterol. Nutr."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1541","DOI":"10.3945\/ajcn.2009.27588","article-title":"Food-based strategies improve iron status in toddlers: A randomized controlled trial","volume":"90","author":"Ferguson","year":"2009","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_14","unstructured":"WHO (2018, April 05). Health Statistics and Information Systems: About the Global Burden of Disease (GBD) Project. Available online: http:\/\/www.who.int\/healthinfo\/global_burden_disease\/about\/en\/."},{"key":"ref_15","first-page":"151","article-title":"Fundamental Principles of Risk Assessment","volume":"Volume 1","author":"Geril","year":"2017","journal-title":"Textbook on Quantitative Tools for Sustainable Food and Energy in the Food Chain"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"647","DOI":"10.1111\/0272-4332.00044","article-title":"Variability and Uncertainty Meet Risk Management and Risk Communication","volume":"22","author":"Thompson","year":"2002","journal-title":"Risk Anal."},{"key":"ref_17","unstructured":"Membr\u00e9, J.M., and Vasilis, V. (2016). Modeling in Food Microbiology, Elsevier."},{"key":"ref_18","unstructured":"ANSES (2017, August 23). Donn\u00e9es de Consommations et Habitudes Alimentaires de L\u2019\u00e9tude INCA 2. Available online: https:\/\/www.data.gouv.fr\/fr\/datasets\/donnees-de-consommations-et-habitudes-alimentaires-de-letude-inca-2-3\/#_."},{"key":"ref_19","unstructured":"Inserm (2019, June 01). M\u00e9nopause: Am\u00e9liorer la S\u00e9curit\u00e9 D\u2019utilisation des Traitements Hormonaux. Available online: https:\/\/www.inserm.fr\/information-en-sante\/dossiers-information\/menopause."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"EFSA Panel on Dietetic Products Nutrition Allergies (2015). Scientific opinion on dietary reference values for iron. EFSA J., 13, 4254.","DOI":"10.2903\/j.efsa.2015.4254"},{"key":"ref_21","unstructured":"Norden (2014). Nordic Nutrition Recommendations 2012: Integrating Nutrition and Physical Activity, Nordic Council of Ministers."},{"key":"ref_22","unstructured":"Ined (2019, June 20). L\u2019\u00e2ge aux Premi\u00e8res R\u00e8gles. Available online: https:\/\/www.ined.fr\/fr\/tout-savoir-population\/memos-demo\/focus\/l-age-aux-premieres-regles\/."},{"key":"ref_23","unstructured":"Stoltzfus, R.J., Mullany, L., and Black, R.E. (2004). Iron Deficiency Anaemia, WHO."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1079\/PHN2001139","article-title":"Iron deficiency in Europe","volume":"4","author":"Hercberg","year":"2001","journal-title":"Public Health Nutr."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1016\/S0338-9898(01)80197-9","article-title":"La dificience en fer et l\u2019an\u00e9mie ferriprive dans la population fran\u00e7aise","volume":"334","author":"Hercberg","year":"2001","journal-title":"Rev. Fran\u00e7aise Lab."},{"key":"ref_26","unstructured":"Sant\u00e9 Publique France-Universit\u00e9 Paris 13 (2006\u20132007). ENNS: \u00c9tude Nationale Nutrition Sant\u00e9, Sant\u00e9 Publique France."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"340","DOI":"10.1038\/ejcn.2010.279","article-title":"Evaluation of iron status in European adolescents through biochemical iron indicators: The HELENA Study","volume":"65","author":"Ferrari","year":"2011","journal-title":"Eur. J. Clin. Nutr."},{"key":"ref_28","unstructured":"Insee (2010). Projections de population 2007-2060 pour la France m\u00e9tropolitaine: Projections de population\u2013Insee R\u00e9sultats, Insee."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"e712","DOI":"10.1016\/S2214-109X(15)00069-8","article-title":"Disability weights for the Global Burden of Disease 2013 study","volume":"3","author":"Salomon","year":"2015","journal-title":"Lancet Glob. Health"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"S684","DOI":"10.1016\/j.fct.2010.05.049","article-title":"BRAFO tiered approach for benefit\u2013risk assessment of foods","volume":"50","author":"Hoekstra","year":"2012","journal-title":"Food Chem. Toxicol."},{"key":"ref_31","unstructured":"ANSES (2019, May 29). Ciqual: Table de Composition Nutritionelle des Aliments. Available online: https:\/\/ciqual.anses.fr\/."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"5S45","DOI":"10.1016\/S0929-693X(17)24009-3","article-title":"Pr\u00e9valence de la carence en fer","volume":"24","author":"Dupont","year":"2017","journal-title":"Arch. P\u00e9diatrie"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"e12460","DOI":"10.1111\/mcn.12460","article-title":"Very low prevalence of iron deficiency among young French children: A national cross-sectional hospital-based survey","volume":"14","author":"Sacri","year":"2018","journal-title":"Matern. Child Nutr."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"192","DOI":"10.1159\/000177811","article-title":"Iron Status of a Healthy French Population: Factors Determining Biochemical Markers","volume":"38","author":"Preziosi","year":"1994","journal-title":"Ann. Nutr. Metab."},{"key":"ref_35","unstructured":"InVS (2019, August 30). Marqueurs Biologiques de L\u2019\u00e9tat Nutritionnel\u2014Adultes 18\u201374 Ans: Tableaux de Distribution\u2014Etude Nationale Nutrition Sant\u00e9 (ENNS). Available online: https:\/\/www.santepubliquefrance.fr\/content\/download\/56036\/file\/etat-nutritionnel-adultes-vitamines-12.pdf."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1038\/sj.ejcn.1600561","article-title":"Determining factors in the iron status of adult women in the SU.VI.MAX study. SUpplementation en VItamines et Min\u00e9raux AntioXydants","volume":"52","author":"Galan","year":"1998","journal-title":"Eur. J. Clin. Nutr."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"859","DOI":"10.1016\/j.foodres.2018.09.021","article-title":"Risk Benefit Assessment of foods: Key findings from an international workshop","volume":"116","author":"Pires","year":"2019","journal-title":"Food Res. Int."},{"key":"ref_38","first-page":"429","article-title":"Quantifying the burden of disease: The technical basis for disability-adjusted life years","volume":"72","author":"Murray","year":"1994","journal-title":"Bull. World Health Organ."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1016\/j.tifs.2018.04.004","article-title":"Meeting the challenges in the development of risk-benefit assessment of foods","volume":"76","author":"Nauta","year":"2018","journal-title":"Trends Food Sci. Technol."},{"key":"ref_40","first-page":"5S18","article-title":"Iron and Neurodevelopment","volume":"24","author":"Vallee","year":"2017","journal-title":"Arch. Pediatr."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1158\/1055-9965.EPI-03-0076","article-title":"Dietary Patterns and Prostate Cancer Risk in the National Health and Nutrition Examination Survey Epidemiological Follow-up Study Cohort","volume":"13","author":"Tseng","year":"2004","journal-title":"Cancer Epidemiol. Biomark. Prev."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1159\/000480742","article-title":"Iron and Cognitive Development: What Is the Evidence?","volume":"71","author":"Larson","year":"2017","journal-title":"Ann. Nutr. Metab."},{"key":"ref_43","unstructured":"IHME (2019, April 22). GBD Compare\/Viz Hub. Available online: https:\/\/vizhub.healthdata.org\/gbd-compare\/."},{"key":"ref_44","unstructured":"FAO\/WHO, and Codex Alimentarius Commission (1999). Principles and Guidelines for the Conduct of Microbiological Risk Assessment, FAO."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1017\/S0950268804001979","article-title":"Disease burden in The Netherlands due to infections with Shiga toxin-producing Escherichia coli O157","volume":"132","author":"Havelaar","year":"2004","journal-title":"Epidemiol. Infect."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"2360","DOI":"10.1111\/risa.12792","article-title":"Development and Application of a Probabilistic Risk-Benefit Assessment Model for Infant Feeding Integrating Microbiological, Nutritional, and Chemical Components","volume":"37","author":"Cummins","year":"2017","journal-title":"Risk Anal."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1016\/j.fct.2018.06.063","article-title":"Investigating the risk-benefit balance of substituting red and processed meat with fish in a Danish diet","volume":"120","author":"Thomsen","year":"2018","journal-title":"Food Chem. Toxicol."},{"key":"ref_48","unstructured":"ANSES (2016). Avis et rapport Relatifs \u00e0 L\u2019actualisation des Rep\u00e8res du PNNS: R\u00e9vision des Rep\u00e8res de Consommation Alimentaires, ANSES."},{"key":"ref_49","unstructured":"WCRF\/AICR (2017). Diet, Nutrition, Physical Activity and Colorectal Cancer, WCRF\/AICR."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1599","DOI":"10.1016\/S1470-2045(15)00444-1","article-title":"Carcinogenicity of consumption of red and processed meat","volume":"16","author":"Bouvard","year":"2015","journal-title":"Lancet Oncol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1016\/j.fct.2019.05.023","article-title":"Estimation of the burden of disease attributable to red meat consumption in France: Influence on colorectal cancer and cardiovascular diseases","volume":"130","author":"Mota","year":"2019","journal-title":"Food Chem. Toxicol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"640","DOI":"10.1158\/1055-9965.EPI-15-0724","article-title":"Heme iron intake, dietary antioxidant capacity, and risk of colorectal adenomas in a large cohort study of French women","volume":"25","author":"Bastide","year":"2016","journal-title":"Cancer Epidemiol. Biomark. Prev."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"870","DOI":"10.1158\/0008-5472.CAN-14-2554","article-title":"A Central Role for Heme Iron in Colon Carcinogenesis Associated with Red Meat Intake","volume":"75","author":"Bastide","year":"2015","journal-title":"Cancer Res."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"969","DOI":"10.1161\/01.CIR.89.3.969","article-title":"Dietary iron intake and risk of coronary disease among men","volume":"89","author":"Ascherio","year":"1994","journal-title":"Circulation"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"101","DOI":"10.2337\/dc06-1686","article-title":"Heme iron from diet as a risk factor for coronary heart disease in women with type 2 diabetes","volume":"30","author":"Qi","year":"2007","journal-title":"Diabetes Care"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"1293","DOI":"10.1016\/S0140-6736(81)92463-6","article-title":"Iron and the sex difference in heart disease risk","volume":"317","author":"Sullivan","year":"1981","journal-title":"Lancet"},{"key":"ref_57","unstructured":"ANSES (2019). Avis de L\u2019AGENCE Nationale de S\u00e9curit\u00e9 Sanitaire de L\u2019alimentation, de L\u2019environnement et du Travail Relatif \u00e0 L\u2019actualisation des Rep\u00e8res Alimentaires du PNNS Pour les Enfants de 4 \u00e0 17 Ans, ANSES."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1079\/BJN19930112","article-title":"Haemoglobin, ferritin, and iron intakes in British children aged 12\u201314 years: A preliminary investigation","volume":"70","author":"Nelson","year":"1993","journal-title":"Br. J. Nutr."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1080\/07315724.1995.10718537","article-title":"Iron and zinc status of young women aged 14 to 19 years consuming vegetarian and omnivorous diets","volume":"14","author":"Donovan","year":"1995","journal-title":"J. Am. Coll. Nutr."},{"key":"ref_60","first-page":"538","article-title":"Nutrient intake and haematological status of vegetarians and age-sex matched omnivores","volume":"48","author":"Alexander","year":"1994","journal-title":"Eur. J. Clin. Nutr."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"65","DOI":"10.3945\/ajcn.112.050609","article-title":"The absorption of iron from whole diets: A systematic review","volume":"98","author":"Collings","year":"2013","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1461S","DOI":"10.3945\/ajcn.2010.28674F","article-title":"Iron bioavailability and dietary reference values","volume":"91","author":"Hurrell","year":"2010","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_63","first-page":"426","article-title":"Effects of iron deficiency anemia on cognitive function in children","volume":"57","author":"Agaoglu","year":"2007","journal-title":"Arzneimittelforschung"},{"key":"ref_64","unstructured":"ECDC\/EFSA (2018). The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-Borne Outbreaks in 2017."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1016\/j.nupar.2019.01.430","article-title":"Risque et b\u00e9n\u00e9fice nutritionnels associ\u00e9s \u00e0 la consommation de viande rouge en France","volume":"33","author":"Mota","year":"2019","journal-title":"Nutr. Clin. M\u00e9tabolisme"}],"container-title":["Nutrients"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-6643\/11\/9\/2045\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T13:15:54Z","timestamp":1760188554000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-6643\/11\/9\/2045"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,9,1]]},"references-count":65,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2019,9]]}},"alternative-id":["nu11092045"],"URL":"https:\/\/doi.org\/10.3390\/nu11092045","relation":{},"ISSN":["2072-6643"],"issn-type":[{"value":"2072-6643","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,9,1]]}}}