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Table 2 Neurodevelopmental outcomes of manganese exposure measured in biomarkers from cross-sectional studies

From: Biomarkers of environmental manganese exposure and associations with childhood neurodevelopment: a systematic review and meta-analysis

Author, Year Age (Years) Country/ Study Name Number (Girls/Boys) Sources Biomarkers Neurological Assessments Associations between Manganese in Biomarkers and Neurodevelopmental Outcomes Adjustment for Covariates Study Quality
Al-Saleh 2019 [40] 0.2–1 Saudi Arabia 206 (96/110) NA Maternal blood and urine, infant urine, breast milk DDST-II, PEDS NS Maternal age and BMI, infant’s age, sex, parity, the location of primary health care centers, maternal education and z score weight for age Medium
Rink 2014 [41] 1.1–3.7 Uruguay 60 (34/26) NA Hair BSID-III H-Mn: NS HOME score, age, child Hb, maternal IQ, SES, Pb, marital status, father education and tester High
Bauer 2017 [42] 10–14 Italy/PHIME 142 (79/63) Fe-Mn alloy plant Teeth VRAM Both low and high prenatal Mn ↓: visuospatial learning and working memory among girls only Sex, age, SES, videogame use, lead, trial and tooth attrition High
Betancourt 2015 [43] 11 Ecuador 93 (46/47) Water consumption from the river Hair PCM H-Mn: ↓: IQ Mother’s literacy Medium
Bhang 2013 [44] 8–11 Korea* 1001 (474/527) NA Blood WASI, ADS, CBCL B-Mn: ↓: academic performance, such as thinking, reading, calculation, lower Mn ↓: attention Age, sex, region, children’s IQ, maternal education and age, levels of cotinine and lead High
Bouchard 2007 [45] 6–15 Canada 46 (22/24) Ground water Hair CPRS-R, CTRS-R H-Mn: ↓: behaviors (teacher-reported hyperactive and oppositional behaviors) Child’s age, sex and income High
Bouchard 2011 [16] 6–13 Canada 362 (194/168) Ground water Hair WASI H-Mn: ↓: IQ Maternal education and IQ, income, home stimulation score, family structure, sex and age of child and IQ testing session, source of water and level of iron in tap water High
Bouchard 2018 [8] 6–14 Canada 259 (132/127) Ground water Hair, saliva, toe nail WISC-IV NS, possible beneficial effects in boys Child’s age, maternal IQ and education, income and IQ tester High
Carvalho 2014 [22] 7–12 Brazil 70 (36/34) Air emissions from Fe-Mn alloy plant Hair WISC-III H-Mn: ↓: estimated IQ, Block Design and Digit Span Maternal education High
Carvalho 2018 [46] 7–12 Brazil 70 (36/34) Air emissions from Fe-Mn alloy plant Hair NEPSY II H-Mn: ↓: verbal memory, behaviors (hyperactivity), not motor Age, sex, SES, mother’s education and mother’s IQ High
Chan 2015 [47] 11–13 USA/NICHD 266 (128/138) NA Teeth DBD NS Child’s race, sex, parental education, marital status and SES High
Chiu 2017 [48] 11–14 Italy/PHIME 194 (105/89) Fe-Mn alloy plant Teeth PA, LNMB Pretnatal T-Mn: ↑: behaviors and motor in boys, T-Mn: ↓: motor (tremor): early postnatal in girls, later postnatal in boys Children’s age and sex, SES index and tooth attrition High
do Nascimento 2015 [49] 6–12 Brazil 69 (34/35) Drinking water from well water Hair, blood RCPM H-Mn: ↓: cognitive function, B-Mn: NS Age, sex and parents’ education High
Ericson 2007 [50] 3–9 USA/SECCYD 27 (16/11) NA Teeth FTT, CBCL Prenatal T-Mn: ↓: behaviors (hyperactivity) Pb, mothers’ education, income and child ethnicity High
Frndak 2019 [51] 6–8 Uruguay 345 (155/190) NA Hair CANTAB, W-M H-Mn: ↑: cognition Child’s age, sex, Pb, hemoglobin, HOME score, crowding, possessions of wealth and mother’s education High
Haynes 2015 [52] 7–9 USA/CARES 404 (187/217) Air-borne Mn from Fe-Mn refinery Hair, blood WISC-IV Both low and high Mn: ↓: IQ Parent IQ Medium
Haynes 2018 [7] 7–9 USA/CARES 106 (65/41) Air-borne Mn from Industry Hair, blood WISC-IV H-Mn: ↓: IQ, B-Mn: NS Parent IQ Medium
Hernandez-Bonilla 2011 [53] 7–11 Mexico 172 (84/88) Air-borne Mn from Mining Hair, blood GP, FT, SA B-Mn: ↓: motor speed and coordination, H-Mn: NS Pb, Hb, sex, age and maternal education High
Hernandez-Bonilla 2016 [54] 7–11 Mexico 267 (136/131) Air-borne Mn from mining district Hair ROCF H-Mn: ↓: visuoperception and short-term visual memory Pb, Hb, child’s age and sex, motor dexterity and mother’s IQ High
Horton 2018 [55] 8–11 Mexico/ELEMENT 133 (69/64) Air pollution and diets Teeth BASC-2 Prenatal T-Mn: ↑: behaviors, postnatal T-Mn: ↓: behaviors (internalizing problems) Maternal education and gestational age High
Khan 2011 [56] 8–11 Bangladesh 201 (100/101) Drinking water from well water Blood CBCL B-Mn: NS Arsenic, sex, BMI, maternal education and arm circumference High
Kicinski 2015 [57] 13.6–17 Belgium 606 (282/324) Low-level metal exposure from industrial areas Blood FT, CPT, DS B-Mn: NS Sex, age, smoking, passive smoking, income, occupation, and maternal education High
Kim 2009 [58] 8–11 Korea 261 (120/141) NA Blood WISC B-Mn: ↓: IQ Age, sex, parental education, income, smoking, birth weight and mother’s age High
Lucchini 2012a [59] 11–14 Italy 299 (147/152) Fe-Mn alloy plant Hair, blood WISC NS Age, sex, BMI, family size, SES, alcohol consumption, area of residence, Hb, ferritin and parity High
Lucchini 2012b [60] 11–14 Italy 311 (153/158) Fe-Mn alloy plant Hair, blood, urine FT, PA, DPD, LNMB B-Mn and H-Mn: ↓: motor (tremor), urine, air, water, diet: NS, soil Mn: ↓: tremor intensity Parity, family size, SES, BMI, maternal education, alcohol intake, smoking, Pb and other metals in air, soil and water. High
Lucchini 2019 [61] 6–12 Italy 299 (161/138) Industrial emission, with potential contamination of environment Hair WISC, CANTAB H-Mn: ↓: working memory Sex, age, maternal IQ and cognitive stimulation besides the confounder distance from the point source High
Menezes-Filho 2011 [21] 6–12 Brazil 83 (39/44) Fe-Mn alloy plant Hair, blood WISC-III H-Mn: ↓: cognition, especially in the verbal domain, B-Mn: NS Maternal education and nutritional status Medium
Menezes-Filho 2014 [62] 7–12 Brazil 70 (36/34) Air-borne Mn from Fe-Mn alloy plant Hair CBCL H-Mn: ↓: behaviors (externalizing behaviors), more pronounced in girls Age, sex and maternal IQ High
Nascimento 2016 [63] 6–12 Brazil 63 (31/32) Potential contamination from pesticide Hair, blood NEUPSILIN-Inf B-Mn: ↓: visual attention, visual perception and phonological awareness, H-Mn: ↓: working memory IQ, age, sex and parents’ education High
Oulhote 2014 [15] 6–13 Canada 375 (200/175) Drinking water from ground water Hair WASI, CPT-II, FT, SA H-Mn: ↓: memory, attention, not hyperactivity, motor: a nonlinear association, ↑: 0.3–0.8 μg/g, ↓: >  10 μg/g, but there were very few observations with such high levels Child’s sex, age, maternal education and IQ, income, maternal depressive symptoms and tap water lead concentrations. High
Parvez 2011 [64] 8–11 Bangladesh 304 (153/151) Drinking water from well water Blood BOT-2 B-Mn: NS Sex, school attendance, head circumference, mother’s intelligence, ferritin, selenium and Pb High
Riojas-Rodríguez 2010 [6] 7–11 Mexico 172 (99/73) Air-borne Mn from mining district Hair, blood WISC H-Mn: ↓: IQ, B-Mn: NS Pb, age, sex, nutritional status, maternal education and IQ High
Rugless 2014 [65] 7–9 USA/CARES 55 (35/20) Air emissions from Fe-Mn refinery Hair, blood APS H-Mn and B-Mn: ↓: postural balance Sex, height/weight ratio, parent IQ, education, Pb and age Medium
Torrente 2005 [66] 12–14 Spain 100 (61/39) Industrial emission Hair AMP H-Mn: NS SES and age Low
Torres-Agustin 2013 [67] 7–11 Mexico 174 (86/88) Air-borne Mn from mining district Hair, blood CAVLT H-Mn: ↓: long-term memory and learning, B-Mn: NS Child’s sex, Pb, age, Hb and maternal education High
Wasserman 2006 [9] 10 Bangladesh 142 (72/70) Drinking water from well water Blood WISC-III B-Mn: NS Maternal education and IQ, house type, family ownership of a television, child height and head circumference High
Wright 2006 [68] 11–13 USA 31 (16/15) Mining waste Hair WASI H-Mn: ↓: Full Scale IQ, Verbal IQ Sex and maternal education Low
  1. *: Effects of pollution on neurobehavioral development, and future policies to protect our children; ↓: Negative association; ↑: Positive association; NA Not available; NS No significant association. Fe-Mn Ferro-manganese; Hb Hemoglobin; Mn Manganese; Pb Lead. B-Mn Manganese in blood; H-Mn Manganese in hair; T-Mn Manganese in teeth. BMI Body mass index; HOME score Home observation for measurement of the environment score; IQ Intelligence Quotient; SES Socioeconomic status. CARES Communities Actively Researching Exposure Study; ELEMENT Early Life Exposures in MExico and NeuroToxicology; NICHD National Institute of Child Health and Human Development; PHIME Public Health Impact of Manganese Exposure in susceptible populations, SECCYD Study of Early Child Care and Youth Development