{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,19]],"date-time":"2026-10-19T16:04:18Z","timestamp":1792425858811,"version":"4.5.0"},"reference-count":40,"publisher":"Springer Science and Business Media LLC","issue":"2","license":[{"start":{"date-parts":[[2020,1,11]],"date-time":"2020-01-11T00:00:00Z","timestamp":1578700800000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"},{"start":{"date-parts":[[2020,1,11]],"date-time":"2020-01-11T00:00:00Z","timestamp":1578700800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Pediatr Res"],"published-print":{"date-parts":[[2020,8]]},"DOI":"10.1038\/s41390-020-0754-4","type":"journal-article","created":{"date-parts":[[2020,1,11]],"date-time":"2020-01-11T14:03:03Z","timestamp":1578751383000},"page":"325-333","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":23,"title":["Modification of the effects of prenatal manganese exposure on child neurodevelopment by maternal anemia and iron deficiency"],"prefix":"10.1038","volume":"88","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8760-2730","authenticated-orcid":false,"given":"Allison","family":"Kupsco","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guadalupe","family":"Estrada-Gutierrez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alejandra","family":"Cantoral","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lourdes","family":"Schnaas","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ivan","family":"Pantic","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chitra","family":"Amarasiriwardena","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katherine","family":"Svensson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David C.","family":"Bellinger","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Martha Mar\u00eda","family":"T\u00e9llez-Rojo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrea A.","family":"Baccarelli","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Robert O.","family":"Wright","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2020,1,11]]},"reference":[{"key":"754_CR1","unstructured":"Freeland-Graves, J. H., Mousa, T. Y., Sanjeevi, N. in Manganese in Health and Disease 34\u201375 (2014). http:\/\/pubs.rsc.org\/en\/content\/chapter\/bk9781849739436-00034\/978-1-84973-943-6"},{"key":"754_CR2","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1098\/rstb.1981.0095","volume":"294","author":"LS Hurley","year":"1981","unstructured":"Hurley, L. S. The role of trace elements in foetal and neonatal development. Philos. Trans. R. Soc. Lond. Ser. B 294, 145\u2013152 (1981).","journal-title":"Philos. Trans. R. Soc. Lond. Ser. B"},{"key":"754_CR3","doi-asserted-by":"publisher","first-page":"93","DOI":"10.1111\/j.1651-2227.1982.tb09605.x","volume":"296","author":"JC Shaw","year":"1982","unstructured":"Shaw, J. C. Trace metal requirements of preterm infants. Acta Paediatr. Scand. Suppl. 296, 93\u2013100 (1982).","journal-title":"Acta Paediatr. Scand. Suppl."},{"key":"754_CR4","doi-asserted-by":"publisher","first-page":"586","DOI":"10.1016\/j.neuro.2011.12.009","volume":"33","author":"CJ Ek","year":"2012","unstructured":"Ek, C. J., Dziegielewska, K. M., Habgood, M. D. & Saunders, N. R. Barriers in the developing brain and neurotoxicology. Neurotoxicology 33, 586\u2013604 (2012).","journal-title":"Neurotoxicology"},{"key":"754_CR5","doi-asserted-by":"publisher","first-page":"688","DOI":"10.1016\/j.envres.2015.09.003","volume":"142","author":"RB Gunier","year":"2015","unstructured":"Gunier, R. B. et al. Manganese in teeth and neurodevelopment in young Mexican\u2013American children. Environ. Res. 142, 688\u2013695 (2015).","journal-title":"Environ. Res."},{"key":"754_CR6","doi-asserted-by":"publisher","first-page":"433","DOI":"10.1097\/EDE.0b013e3181df8e52","volume":"21","author":"BC Henn","year":"2010","unstructured":"Henn, B. C. et al. Early postnatal blood manganese levels and children\u2019s neurodevelopment. Epidemiology 21, 433\u2013439 (2010).","journal-title":"Epidemiology"},{"key":"754_CR7","unstructured":"Mu\u00f1oz-Rocha, T. V. et al. Prenatal co-exposure to manganese and depression and 24-months neurodevelopment. Neurotoxicology (2017). http:\/\/www.sciencedirect.com\/science\/article\/pii\/S0161813X17301201"},{"key":"754_CR8","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1016\/j.envint.2015.07.009","volume":"84","author":"AM Mora","year":"2015","unstructured":"Mora, A. M. et al. Prenatal and postnatal manganese teeth levels and neurodevelopment at 7, 9, and 10.5 years in the CHAMACOS cohort. Environ. Int. 84, 39\u201354 (2015).","journal-title":"Environ. Int."},{"key":"754_CR9","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1016\/j.neuro.2013.06.002","volume":"38","author":"YA Seo","year":"2013","unstructured":"Seo, Y. A., Li, Y. & Wessling-Resnick, M. Iron depletion increases manganese uptake and potentiates apoptosis through ER stress. Neurotoxicology 38, 67\u201373 (2013).","journal-title":"Neurotoxicology"},{"key":"754_CR10","volume-title":"Iron Deficiency Anaemia: Assessment, Prevention, and Control: A Guide For Programme Managers","author":"World Health Organization.","year":"2001","unstructured":"World Health Organization. Iron Deficiency Anaemia: Assessment, Prevention, and Control: A Guide For Programme Managers (WHO, Geneva, Switzerland, 2001)."},{"key":"754_CR11","doi-asserted-by":"publisher","first-page":"571","DOI":"10.1038\/ijo.2015.3","volume":"39","author":"L Garcia-Valdes","year":"2015","unstructured":"Garcia-Valdes, L. et al. The impact of maternal obesity on iron status, placental transferrin receptor expression and hepcidin expression in human pregnancy. Int. J. Obes. 39, 571\u2013578 (2015).","journal-title":"Int. J. Obes."},{"key":"754_CR12","doi-asserted-by":"publisher","first-page":"2123","DOI":"10.1016\/S0140-6736(10)62304-5","volume":"378","author":"Y Balarajan","year":"2011","unstructured":"Balarajan, Y., Ramakrishnan, U., \u00d6zaltin, E., Shankar, A. H. & Subramanian, S. V. Anaemia in low-income and middle-income countries. Lancet 378, 2123\u20132135 (2011).","journal-title":"Lancet"},{"key":"754_CR13","unstructured":"Claus Henn, B et al. Maternal and cord blood manganese concentrations and early childhood neurodevelopment among residents near a mining-impacted superfund site. Environ. Health Perspect. (2017). https:\/\/www.ncbi.nlm.nih.gov\/pmc\/articles\/PMC5743453\/"},{"key":"754_CR14","doi-asserted-by":"publisher","first-page":"126","DOI":"10.1289\/ehp.1003300","volume":"120","author":"BC Henn","year":"2012","unstructured":"Henn, B. C. et al. Associations of early childhood manganese and lead coexposure with neurodevelopment. Environ. Health Perspect. 120, 126\u2013131 (2012).","journal-title":"Environ. Health Perspect."},{"key":"754_CR15","doi-asserted-by":"publisher","first-page":"486","DOI":"10.1038\/sj.ejcn.1600781","volume":"53","author":"M Krachler","year":"1999","unstructured":"Krachler, M., Rossipal, E. & Micetic-Turk, D. Trace element transfer from the mother to the newborn\u2014investigations on triplets of colostrum, maternal and umbilical cord sera. Eur. J. Clin. Nutr. 53, 486\u2013494 (1999).","journal-title":"Eur. J. Clin. Nutr."},{"key":"754_CR16","doi-asserted-by":"publisher","DOI":"10.1186\/1476-069X-13-50","volume":"13","author":"JM Braun","year":"2014","unstructured":"Braun, J. M. et al. Relationships between lead biomarkers and diurnal salivary cortisol indices in pregnant women from Mexico City: a cross-sectional study. Environ. Health 13, 50 (2014).","journal-title":"Environ. Health"},{"key":"754_CR17","doi-asserted-by":"publisher","first-page":"271","DOI":"10.2217\/epi.13.24","volume":"5","author":"HH Burris","year":"2013","unstructured":"Burris, H. H. et al. Association between birth weight and DNA methylation of IGF2, glucocorticoid receptor and repetitive elements LINE-1 and Alu. Epigenomics 5, 271\u2013281 (2013).","journal-title":"Epigenomics"},{"key":"754_CR18","doi-asserted-by":"publisher","first-page":"177","DOI":"10.1111\/j.1751-553X.2008.01067.x","volume":"30","author":"JA Leifert","year":"2008","unstructured":"Leifert, J. A. Anaemia and cigarette smoking. Int. J. Lab. Hematol. 30, 177\u2013184 (2008).","journal-title":"Int. J. Lab. Hematol."},{"key":"754_CR19","doi-asserted-by":"publisher","first-page":"207","DOI":"10.1086\/660885","volume":"5","author":"GL Wehby","year":"2011","unstructured":"Wehby, G. L., Prater, K., McCarthy, A. M., Castilla, E. E. & Murray, J. C. The impact of maternal smoking during pregnancy on early child neurodevelopment. J. Hum. Cap. 5, 207\u2013254 (2011).","journal-title":"J. Hum. Cap."},{"key":"754_CR20","doi-asserted-by":"publisher","first-page":"226","DOI":"10.1016\/j.envres.2016.10.014","volume":"152","author":"S Renzetti","year":"2017","unstructured":"Renzetti, S. et al. The association of lead exposure during pregnancy and childhood anthropometry in the Mexican PROGRESS cohort. Environ. Res. 152, 226\u2013232 (2017).","journal-title":"Environ. Res."},{"key":"754_CR21","unstructured":"McCarthy, D. Manual for the McCarthy Scales of Children\u2019s Abilities. New York, Psychological Corporation, 1972."},{"key":"754_CR22","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1590\/S0036-36341998000200005","volume":"40","author":"M Hern\u00e1ndez-Avila","year":"1998","unstructured":"Hern\u00e1ndez-Avila, M. et al. Validity and reproducibility of a food frequency questionnaire to assess dietary intake of women living in Mexico City. Sal. Pub. Mex. 40, 133\u2013140 (1998).","journal-title":"Sal. Pub. Mex."},{"key":"754_CR23","unstructured":"Malin, A. J. et al. Quality of prenatal and childhood diet predicts neurodevelopmental outcomes among children in Mexico City. Nutrients (2018). https:\/\/www.ncbi.nlm.nih.gov\/pmc\/articles\/PMC6115750\/"},{"issue":"Suppl. 4","key":"754_CR24","first-page":"S523","volume":"51","author":"S Rodr\u00edguez-Ram\u00edrez","year":"2009","unstructured":"Rodr\u00edguez-Ram\u00edrez, S., Mundo-Rosas, V., Jim\u00e9nez-Aguilar, A. & Shamah-Levy, T. Methodology for the analysis of dietary data from the Mexican National Health and Nutrition Survey 2006. Sal. Pub. Mex. 51(Suppl. 4), S523\u2013S529 (2009).","journal-title":"Sal. Pub. Mex."},{"key":"754_CR25","first-page":"625","volume":"48","author":"H Dirren","year":"1994","unstructured":"Dirren, H., Logman, M. H., Barclay, D. V. & Freire, W. B. Altitude correction for hemoglobin. Eur. J. Clin. Nutr. 48, 625\u2013632 (1994).","journal-title":"Eur. J. Clin. Nutr."},{"key":"754_CR26","unstructured":"Carrasco, A. V. The AMAI System of Classifying Households by Socio-economic Level: The experience of Mexico and its comparison with Brazil and Argentina (ESOMAR, 2002)."},{"key":"754_CR27","unstructured":"R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, Austria, 2018). https:\/\/www.R-project.org\/"},{"key":"754_CR28","doi-asserted-by":"publisher","first-page":"52","DOI":"10.1016\/j.envres.2013.03.003","volume":"123","author":"C-C Lin","year":"2013","unstructured":"Lin, C.-C. et al. In utero exposure to environmental lead and manganese and neurodevelopment at 2 years of age. Environ. Res. 123, 52\u201357 (2013).","journal-title":"Environ. Res."},{"key":"754_CR29","doi-asserted-by":"publisher","first-page":"667","DOI":"10.1016\/S0161-813X(03)00058-5","volume":"24","author":"L Takser","year":"2003","unstructured":"Takser, L., Mergler, D., Hellier, G., Sahuquillo, J. & Huel, G. Manganese, monoamine metabolite levels at birth, and child psychomotor development. Neurotoxicology 24, 667\u2013674 (2003).","journal-title":"Neurotoxicology"},{"key":"754_CR30","doi-asserted-by":"publisher","first-page":"333","DOI":"10.1016\/S0149-7634(05)80026-0","volume":"15","author":"M Aschner","year":"1991","unstructured":"Aschner, M. & Aschner, J. L. Manganese neurotoxicity: cellular effects and blood-brain barrier transport. Neurosci. Biobehav. Rev. 15, 333\u2013340 (1991).","journal-title":"Neurosci. Biobehav. Rev."},{"key":"754_CR31","doi-asserted-by":"publisher","first-page":"2282","DOI":"10.1093\/jn\/127.12.2282","volume":"127","author":"C Nelson","year":"1997","unstructured":"Nelson, C., Erikson, K., Pi\u00f1ero, D. J. & Beard, J. L. In vivo dopamine metabolism is altered in iron-deficient anemic rats. J. Nutr. 127, 2282\u20132288 (1997).","journal-title":"J. Nutr."},{"key":"754_CR32","doi-asserted-by":"publisher","first-page":"1101","DOI":"10.1016\/j.jnutbio.2014.07.003","volume":"25","author":"J Kim","year":"2014","unstructured":"Kim, J. & Wessling-Resnick, M. Iron and mechanisms of emotional behavior. J. Nutr. Biochem. 25, 1101\u20131107 (2014).","journal-title":"J. Nutr. Biochem."},{"key":"754_CR33","doi-asserted-by":"publisher","first-page":"959","DOI":"10.2165\/00003088-200241120-00003","volume":"41","author":"J Alcorn","year":"2002","unstructured":"Alcorn, J. & McNamara, P. J. Ontogeny of hepatic and renal systemic clearance pathways in infants. Part I. Clin. Pharmacokinet. 41, 959\u2013998 (2002).","journal-title":"Clin. Pharmacokinet."},{"key":"754_CR34","doi-asserted-by":"publisher","first-page":"891","DOI":"10.2217\/whe.15.35","volume":"11","author":"GC Di Renzo","year":"2015","unstructured":"Di Renzo, G. C. et al. Iron deficiency anemia in pregnancy. Women\u2019s Health (Lond. Engl.) 11, 891\u2013900 (2015).","journal-title":"Women\u2019s Health (Lond. Engl.)"},{"key":"754_CR35","doi-asserted-by":"publisher","first-page":"293","DOI":"10.1016\/j.neuro.2013.09.006","volume":"45","author":"JA Menezes-Filho","year":"2014","unstructured":"Menezes-Filho, J. A. et al. Elevated manganese exposure and school-aged children\u2019s behavior: a gender-stratified analysis. Neurotoxicology 45, 293\u2013300 (2014).","journal-title":"Neurotoxicology"},{"key":"754_CR36","doi-asserted-by":"publisher","first-page":"367","DOI":"10.1097\/EDE.0b013e31819b93c0","volume":"20","author":"AR Zota","year":"2009","unstructured":"Zota, A. R. et al. Maternal blood manganese levels and infant birth weight. Epidemiology 20, 367\u2013373 (2009).","journal-title":"Epidemiology"},{"key":"754_CR37","doi-asserted-by":"publisher","first-page":"1322","DOI":"10.1039\/b903805a","volume":"11","author":"CV Rudge","year":"2009","unstructured":"Rudge, C. V. et al. The placenta as a barrier for toxic and essential elements in paired maternal and cord blood samples of South African delivering women. J. Environ. Monit. 11, 1322\u20131330 (2009).","journal-title":"J. Environ. Monit."},{"key":"754_CR38","doi-asserted-by":"publisher","first-page":"256","DOI":"10.1016\/j.ntt.2009.08.010","volume":"32","author":"N Abdelouahab","year":"2010","unstructured":"Abdelouahab, N. et al. Monoamine oxidase activity in placenta in relation to manganese, cadmium, lead, and mercury at delivery. Neurotoxicol. Teratol. 32, 256\u2013261 (2010).","journal-title":"Neurotoxicol. Teratol."},{"key":"754_CR39","unstructured":"Shamah-Levy, T. et al. Tendencia en la prevalencia de anemia entre mujeres mexicanas en edad reproductiva 2006-2016. Ensanut MC 2016. Sal. P\u00fab. M\u00e9x. 60, 301\u2013308 (2018)."},{"key":"754_CR40","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1093\/ajcn\/70.1.37","volume":"70","author":"JW Finley","year":"1999","unstructured":"Finley, J. W. Manganese absorption and retention by young women is associated with serum ferritin concentration. Am. J. Clin. Nutr. 70, 37\u201343 (1999).","journal-title":"Am. J. Clin. Nutr."}],"container-title":["Pediatric Research"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/www.nature.com\/articles\/s41390-020-0754-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/s41390-020-0754-4","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/s41390-020-0754-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,5,20]],"date-time":"2023-05-20T21:29:56Z","timestamp":1684618196000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41390-020-0754-4"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,1,11]]},"references-count":40,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2020,8]]}},"alternative-id":["754"],"URL":"https:\/\/doi.org\/10.1038\/s41390-020-0754-4","relation":{},"ISSN":["0031-3998","1530-0447"],"issn-type":[{"value":"0031-3998","type":"print"},{"value":"1530-0447","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,1,11]]},"assertion":[{"value":"16 August 2019","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"22 November 2019","order":2,"name":"revised","label":"Revised","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"29 December 2019","order":3,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"11 January 2020","order":4,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}]}}