{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T19:42:40Z","timestamp":1760211760153,"version":"build-2065373602"},"reference-count":56,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2016,7,26]],"date-time":"2016-07-26T00:00:00Z","timestamp":1469491200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000066","name":"National Institute of Environmental Health Sciences","doi-asserted-by":"publisher","award":["R01-ES018858","1K02-ES019878-01","K01-ES015 877"],"award-info":[{"award-number":["R01-ES018858","1K02-ES019878-01","K01-ES015 877"]}],"id":[{"id":"10.13039\/100000066","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJERPH"],"abstract":"<jats:p>Background: Still considered one of the most prevalent nutritional problems in the world, anemia has been shown in many studies to have deleterious effects on neurobehavioral development. While most research efforts have focused on investigating the effects of anemia on social and emotional development of infants by using a cross-sectional design, research is still needed to investigate whether early childhood anemia, beyond infantile years, is linked with behavioral problems. Objective: This study assessed whether (1) hemoglobin (Hb) levels in early childhood are associated with externalizing behavior; and (2) this relationship is confounded by social adversity. Methods: Hemoglobin levels were taken from children (N = 98) of the China Jintan Cohort Study at age 4 years, and externalizing behaviors (attention and aggression) were assessed with the Child Behavior Checklist (ASEBA-CBCL) at age 6 years (mean age 5.77 \u00b1 0.39 years old). Results: Compared with other children in the sample, children with relatively lower Hb levels at age 4 had more behavioral problems in both attention and aggression at age 6, independent of social adversity. For boys, this association was significant for attention problems, which did not interact with social adversity. For girls, the association was significant for aggression, which interacted with social adversity. While girls on average exhibited higher social adversity than boys, the main effect of Hb was only significant in girls with low social adversity. Conclusions: These results indicate that there is an inverse association between hemoglobin levels and later behavioral problems. Findings of this study suggest that regular monitoring of children\u2019s hemoglobin levels and appropriate intervention may help with early identification of behavioral problems.<\/jats:p>","DOI":"10.3390\/ijerph13080758","type":"journal-article","created":{"date-parts":[[2016,7,26]],"date-time":"2016-07-26T10:34:47Z","timestamp":1469529287000},"page":"758","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":7,"title":["Hemoglobin Status and Externalizing Behavioral Problems in Children"],"prefix":"10.3390","volume":"13","author":[{"given":"Jianhua","family":"Su","sequence":"first","affiliation":[{"name":"Department of Neurology, The Jintan Hospital Affiliated to Jiangsu University, 16 Nanmen Street, Jintan, Changzhou 213200, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Naixue","family":"Cui","sequence":"additional","affiliation":[{"name":"Schools of Nursing and Medicine, University of Pennsylvania, 418 Curie Blvd., Room 426, Claire M. Fagin Hall, Philadelphia, PA 19104, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Guoping","family":"Zhou","sequence":"additional","affiliation":[{"name":"Department of Neurology, The Jintan Hospital Affiliated to Jiangsu University, 16 Nanmen Street, Jintan, Changzhou 213200, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yuexian","family":"Ai","sequence":"additional","affiliation":[{"name":"Department of Neurology, The Jintan Hospital Affiliated to Jiangsu University, 16 Nanmen Street, Jintan, Changzhou 213200, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Guiju","family":"Sun","sequence":"additional","affiliation":[{"name":"Department of Nutrition and Food Hygiene, School of Public Health, Southeast University, Room #508, 87, DingJiaqiao, Nanjing 210096, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sophie","family":"Zhao","sequence":"additional","affiliation":[{"name":"Schools of Nursing and Medicine, University of Pennsylvania, 418 Curie Blvd., Room 426, Claire M. Fagin Hall, Philadelphia, PA 19104, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8405-6153","authenticated-orcid":false,"given":"Jianghong","family":"Liu","sequence":"additional","affiliation":[{"name":"Schools of Nursing and Medicine, University of Pennsylvania, 418 Curie Blvd., Room 426, Claire M. Fagin Hall, Philadelphia, PA 19104, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2016,7,26]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1177\/156482650502600108","article-title":"Recent trends in malnutrition in developing regions: Vitamin A deficiency, anemia, iodine deficiency, and child underweight","volume":"26","author":"Mason","year":"2005","journal-title":"Food Nutr. Bull."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1007\/s00277-010-1144-5","article-title":"Anemia\u2014Still a major health problem in many parts of the world!","volume":"90","author":"Milman","year":"2011","journal-title":"Ann. Hematol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1159\/000345167","article-title":"Global nutrition epidemiology and trends","volume":"61","author":"Bhutta","year":"2012","journal-title":"Ann. Nutr. Metab."},{"key":"ref_4","first-page":"886","article-title":"Prevalence of iron deficiency in children aged 7 months to 7 years in China","volume":"42","author":"Zhu","year":"2004","journal-title":"Chin. J. Pediatr."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"412","DOI":"10.1159\/000075667","article-title":"Perinatal iron deficiency alters apical dendritic growth in hippocampal CA1 pyramidal neurons","volume":"25","author":"Jorgenson","year":"2003","journal-title":"Dev. Neurosci. Baseline"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"3215","DOI":"10.1093\/jn\/133.10.3215","article-title":"Perinatal iron deficiency alters the neurochemical profile of the developing rat hippocampus","volume":"133","author":"Rao","year":"2003","journal-title":"J. Nutr."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Uematsu, A., Matsui, M., Tanaka, C., Takahashi, T., Noguchi, K., Suzuki, M., and Nishijo, H. (2012). Developmental trajectories of amygdala and hippocampus from infancy to early adulthood in healthy individuals. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0046970"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1007\/BF03033574","article-title":"Brain iron deficiency and excess; cognitive impairment and neurodegeneration with involvement of striatum and hippocampus","volume":"14","author":"Youdim","year":"2008","journal-title":"Neurotox. Res."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1007\/BF02725658","article-title":"Role of micronutrients for physical growth and mental development","volume":"71","author":"Singh","year":"2004","journal-title":"Indian J. Pediatr."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1097\/01.mop.0000245360.13949.91","article-title":"The effect of childhood malnutrition on externalizing behavior","volume":"18","author":"Liu","year":"2006","journal-title":"Curr. Opin. Pediatr."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"740S","DOI":"10.3945\/jn.110.131169","article-title":"Early iron deficiency has brain and behavior effects consistent with dopaminergic dysfunction","volume":"141","author":"Lozoff","year":"2011","journal-title":"J. Nutr."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"649S","DOI":"10.1093\/jn\/131.2.649S","article-title":"A review of studies on the effect of iron deficiency on cognitive development in children","volume":"131","author":"Ani","year":"2001","journal-title":"J. Nutr."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1159\/000334490","article-title":"The effect of iron on cognitive development and function in infants, children and adolescents: A systematic review","volume":"59","author":"Hermoso","year":"2011","journal-title":"Ann. Nutr. Metab."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1001\/archpedi.157.6.593","article-title":"Malnutrition at age 3 years and lower cognitive ability at age 11 years: Independence from psychosocial adversity","volume":"157","author":"Liu","year":"2003","journal-title":"Arch. Pediatr. Adolesc. Med."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1471-244X-13-161","article-title":"Association between psychiatric disorders and iron deficiency anemia among children and adolescents: A nationwide population-based study","volume":"13","author":"Chen","year":"2013","journal-title":"BMC Psychiatry"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1016\/j.pediatrneurol.2007.08.014","article-title":"Effects of iron supplementation on attention deficit hyperactivity disorder in children","volume":"38","author":"Konofal","year":"2008","journal-title":"Pediatr. Neurol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"E51","DOI":"10.1542\/peds.105.4.e51","article-title":"Poorer behavioral and developmental outcome more than 10 years after treatment for iron deficiency in infancy","volume":"105","author":"Lozoff","year":"2000","journal-title":"Pediatrics"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1016\/S0022-3476(83)80177-2","article-title":"Effect of mild iron deficiency on infant mental development scores","volume":"102","author":"Walter","year":"1983","journal-title":"J. Pediatr."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1542\/peds.84.1.7","article-title":"Iron deficiency anemia: Adverse effects on infant psychomotor development","volume":"84","author":"Walter","year":"1989","journal-title":"Pediatrics"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1097\/00004703-198606000-00004","article-title":"Iron-deficient anemic infants at play","volume":"7","author":"Lozoff","year":"1986","journal-title":"J. Dev. Behav. Pediatr."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1179\/147683008X301568","article-title":"Long-lasting cognitive, physiological and hematological effects in rehabilitated, early dietary iron-deficiency adult rats, and improvement by treatment with a mixture of essential fatty acids","volume":"11","author":"Yehuda","year":"2008","journal-title":"Nutr. Neurosci."},{"key":"ref_22","first-page":"24","article-title":"Behavior of infants with iron-deficiency anemia","volume":"69","author":"Lozoff","year":"1998","journal-title":"Child Dev."},{"key":"ref_23","first-page":"487","article-title":"Iron deficiency and psychomotor development scores: A longitudinal study between ages 10 months and 4 years","volume":"46","author":"Dommergues","year":"1989","journal-title":"Arch. Fr. Pediatr."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"683","DOI":"10.1093\/jn\/137.3.683","article-title":"Preschool-aged children with iron deficiency anemia show altered affect and behavior","volume":"137","author":"Lozoff","year":"2007","journal-title":"J. Nutr."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1179\/147683011X13009738172521","article-title":"Early malnutrition predicts parent reports of externalizing behaviors at ages 9\u201317","volume":"14","author":"Galler","year":"2011","journal-title":"Nutr. Neurosci."},{"key":"ref_26","unstructured":"Achenbach, T.M. (1991). Manual for the Child Behavior Checklist\/4\u201318 and 1991 Profile, Department of Psychiatry, University of Vermont."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"788","DOI":"10.3945\/jn.111.145441","article-title":"Infant malnutrition is associated with persisting attention deficits in middle adulthood","volume":"142","author":"Galler","year":"2012","journal-title":"J. Nutr."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1111\/1469-7610.00034","article-title":"Annotation: The role of prefrontal deficits, low autonomic arousal, and early health factors in the development of antisocial and aggressive behavior in children","volume":"43","author":"Raine","year":"2002","journal-title":"J. Child Psychol. Psychiatry"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1016\/j.ijnurstu.2004.06.007","article-title":"Biosocial bases of aggressive and violent behavior\u2014Implications for nursing studies","volume":"42","author":"Liu","year":"2005","journal-title":"Int. J. Nurs Stud."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"674","DOI":"10.1037\/0033-295X.100.4.674","article-title":"Adolescence-limited and life-course-persistent antisocial behavior: A developmental taxonomy","volume":"100","author":"Moffitt","year":"1993","journal-title":"Psychol. Rev."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/j.avb.2010.12.003","article-title":"Early health risk factors for violence: Conceptualization, review of the evidence, and implications","volume":"16","author":"Liu","year":"2011","journal-title":"Aggress. Violent Behav."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1002\/yd.20009","article-title":"Risk and protective factors, longitudinal research, and bullying prevention","volume":"2012","author":"Ttofi","year":"2012","journal-title":"New Dir. Youth Dev."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"530","DOI":"10.3390\/nu6020530","article-title":"Low blood zinc, iron, and other sociodemographic factors associated with behavior problems in preschoolers","volume":"6","author":"Liu","year":"2014","journal-title":"Nutrients"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Liu, J., Cao, S., Chen, Z., Raine, A., Hanlon, A., Ai, Y., Zhou, G., Yan, C., Leung, P., and McCauley, L. (2015). Cohort profile update: The China Jintan child cohort study. Int. J. Epidemiol.","DOI":"10.1093\/ije\/dyv119"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"668","DOI":"10.1093\/ije\/dyp205","article-title":"Cohort profile: The China Jintan child cohort study","volume":"39","author":"Liu","year":"2010","journal-title":"Int. J. Epidemiol."},{"key":"ref_36","unstructured":"Achenbach, T., and Rescorla, L. (2001). Manual for the ASEBA Preschool Forms & Profiles, Research Center for Children, Youth, & Familly, University of Vermont."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"904","DOI":"10.1016\/j.ijnurstu.2011.04.003","article-title":"Community-based participatory research (CBPR) approach to study children\u2019s health in China: Experiences and reflections","volume":"48","author":"Liu","year":"2011","journal-title":"Int. J. Nurs. Stud."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1007\/s10802-010-9452-8","article-title":"The application of the preschool child behavior checklist and the caregiver-teacher report form to mainland Chinese children: Syndrome structure, gender differences, country effects, and inter-informant agreement","volume":"39","author":"Liu","year":"2011","journal-title":"J. Abnorm. Child Psychol."},{"key":"ref_39","first-page":"95","article-title":"Family, area and school influences in the genesis of conduct disorders","volume":"1","author":"Rutter","year":"1978","journal-title":"Book Suppl. J. Child Psychol. Psychiatr."},{"key":"ref_40","unstructured":"Tonry, M. (1990). Crime and Justice: A Review of Research, University of Chicago Press."},{"key":"ref_41","unstructured":"Siberry, G.K., and Iannone, R. (2000). The Harriet Lane Handbook: A Manual for Pediatric House Officers, Mosby Year Book. [15th ed.]."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"S34","DOI":"10.1301\/nr.2006.may.S34-S43","article-title":"Long-lasting neural and behavioral effects of iron deficiency in infancy","volume":"64","author":"Lozoff","year":"2006","journal-title":"Nutr. Rev."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"480","DOI":"10.1136\/adc.84.6.480","article-title":"Should infants be screened for anaemia? A prospective study investigating the relation between haemoglobin at 8, 12, and 18 months and development at 18 months","volume":"84","author":"Sherriff","year":"2001","journal-title":"Arch. Dis. Child"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1080","DOI":"10.1007\/s10995-012-1090-z","article-title":"Iron deficiency after arrival is associated with general cognitive and behavioral impairment in post-institutionalized children adopted from Eastern Europe","volume":"17","author":"Fuglestad","year":"2013","journal-title":"Matern. Child Health J."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"S64","DOI":"10.1111\/j.1753-4887.2011.00435.x","article-title":"Iron deficiency and iron-deficiency anemia in the first two years of life: Strategies to prevent loss of developmental potential","volume":"69","author":"Black","year":"2011","journal-title":"Nutr. Rev."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"254","DOI":"10.1097\/00004583-198903000-00018","article-title":"A follow-up study of the influence of early malnutrition on subsequent development. Home and classroom behavior","volume":"28","author":"Galler","year":"1989","journal-title":"J. Am. Acad. Child Adolesc. Psychiatry"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1046\/j.1467-0658.2001.00109.x","article-title":"Children and famine: Long-term effects on behavioral development","volume":"7","author":"Galler","year":"2002","journal-title":"Ambul. Child Health"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1203\/01.PDR.0000047657.23156.55","article-title":"Iron deficiency anemia in infancy: Long-lasting effects on auditory and visual system functioning","volume":"53","author":"Algarin","year":"2003","journal-title":"Pediatr. Res."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1007\/s12098-010-0192-0","article-title":"Developmental and neurophysiologic deficits in iron deficiency in children","volume":"78","author":"Madan","year":"2011","journal-title":"Indian J. Pediatr."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.neuroscience.2013.07.058","article-title":"Iron deficiency alters expression of dopamine-related genes in the ventral midbrain in mice","volume":"252","author":"Jellen","year":"2013","journal-title":"Neuroscience"},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Feinman, S., Roberts, D., Hsieh, K.F., Sawyer, D., and Swanson, D. (1992). A Critical Review of Social Referencing in Infancy, Plenum Press.","DOI":"10.1007\/978-1-4899-2462-9_2"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"626","DOI":"10.2307\/1130562","article-title":"A descriptive analysis of infant social referencing","volume":"59","author":"Hornik","year":"1988","journal-title":"Child Dev."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"536","DOI":"10.1016\/j.infbeh.2014.06.004","article-title":"Social looking, social referencing and humor perception in 6-and-12-month-old infants","volume":"37","author":"Mireault","year":"2014","journal-title":"Infant Behav. Dev."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1901\/jaba.2012.45-23","article-title":"Acquisition of social referencing via discrimination training in infants","volume":"45","author":"Pelaez","year":"2012","journal-title":"J. Appl. Behav. Anal."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1097\/00004703-200610000-00001","article-title":"Iron deficiency in infancy and mother-child interaction at 5 years","volume":"27","author":"Corapci","year":"2006","journal-title":"J. Dev. Behav. Pediatr."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"2005","DOI":"10.1176\/appi.ajp.161.11.2005","article-title":"Malnutrition at age 3 years and externalizing behavior problems at ages 8, 11, and 17 years","volume":"161","author":"Liu","year":"2004","journal-title":"Am. J. Psychiatry"}],"container-title":["International Journal of Environmental Research and Public Health"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1660-4601\/13\/8\/758\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T19:27:04Z","timestamp":1760210824000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1660-4601\/13\/8\/758"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,7,26]]},"references-count":56,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2016,8]]}},"alternative-id":["ijerph13080758"],"URL":"https:\/\/doi.org\/10.3390\/ijerph13080758","relation":{},"ISSN":["1660-4601"],"issn-type":[{"type":"electronic","value":"1660-4601"}],"subject":[],"published":{"date-parts":[[2016,7,26]]}}}