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Table 1 Summary of study characteristics

From: Measuring the impact of manganese exposure on children’s neurodevelopment: advances and research gaps in biomarker-based approaches

Study Author Date of Publication Country Study design Study Population Sample size Environ-mental Mn Measure Biomarker Measure Neurodevelopmental Outcome
Barlow et al. (1983) [62] United Kingdom Case control Children ≤ 16 years 68 exposed (65 controls) None measured Hair Diagnosis of hyperactivity by personal physicians, child psychiatrists and social workers
Collipp et al. (1983) [34] Long Island, New York, US Cross-sectional Infants and children ≤ 4 years 70 Infant formula Hair No health outcome
   Case control Learning disabled children and controls 7–10 years 16 learning disabled children; (44 controls)   Hair Learning disability for 7-10 year olds (parent and teacher reports, child interview, and neurological exam)
Takser et al. (2003) [43] Paris, France Prospective Mother-infant pairs followed until 6 years 247 mother- infant pairs, 100 after 6 years) None measured Hair, cord blood, placenta Attention, nonverbal memory, hand skills, general psychomotor indices (Brunet-Lézine development quotient at 9 months), (McCarthy General Cognitive Index at 3 and 6 years)
Wasserman et al. (2006) [18] Araihazar Bangladesh Cross sectional Children 9.5–10.5 years 142 Well water Blood IQ (Wechsler Intelligence Scale for Children, WISC-III)
Wright et al. (2006) [16] Miami, OK, US Cross sectional Children 11–13 years 31 Not measured, but location coexisted with a Superfund site (Pb, Zn, Mn, Cd) Hair IQ (Wechsler Abbreviated Scale of Intelligence or WASI); Wide Range Assessment of Visual Motor Ability; receptive scales of Clinical Evaluation of Language Fundamentals; California Verbal Learning Test-Children; Behavioral Assessment System for Children; tests of story memory (Wide Range Assessment of Memory and Learning); Children’s Depression Inventory, and the Behavior Rating Inventory of Executive Functions
Bouchard et al. (2007) [17] Québec, Canada Cross sectional Children 6–15
years
46 Well water Hair Hyperactivity, oppositional behavior, cognitive problems, inattention, (Revised Conners Teachers’ and Parents’ Rating Scales)
Ericson et al. (2007) [52] United States Prospective NICHD Study of Early Child Care and Youth Development who shed a tooth 27 None measured Tooth enamel Behavioral disinhibition (Forbidden Toy Task), sustained attention (Mirsky Continuous Performance Test), impulsive error score (Children’s Stroop Test), and total, internalizing, externalizing and attention problems (Children Behavior Checklist)
Kim et al. (2009) [26] Seoul, Seongnam, Ulsan, and Yeoncheon, South Korea Cross sectional Children 8–11 years 261 None measured Blood IQ including vocabulary, arithmetic, picture arrangement and block design (Korean Educational Development Institute-Wechsler Intelligence Scales)
Claus Henn et al. (2010) [44] Mexico City, Mexico Prospective Children enrolled at or before birth and followed through age 3 448 None measured Blood Mental Development Index (MDI) and the Psychomotor Development Index (PDI) (Bayley Scales of Infant Development-II)
Riojas- Rodriguez et al. (2010) [31] Hidalgo, Mexico Cross sectional Children 7–11 years 79 (93 controls) None measured Hair, blood IQ (WISC-Revised)
Bouchard et al. (2011) [32] Québec, Canada Cross sectional Children 6–13 years 362 Water, diet Hair IQ (WASI)
Hernández-Bonilla et al. (2011) [48] Hidalgo, Mexico Cross sectional Children 7–11 years 100 exposed (95 controls) Prior studies show airborne Mn levels (median 0.10 g/m3) exceed 2006 US EPA Reference Concentration (0.05 μg/m3) Hair, blood Motor function: grooved pegboard, finger tapping, and Santa Ana test
Khan et al. (2011) [29] Araihazar Bangladesh Cross sectional Children 8–11 years 201 Water Blood Child behaviors including internalizing and externalizing subscales and a total score (TRF Achenbach System of Empirically Based Assessment)
Menezes-Filho et al. (2011) [35] Salvador, Brazil Cross sectional Children 6–12 years 83 None measured Hair, blood IQ (WISC - III)
Parvez et al. (2011) [49] Araihazar Bangladesh Cross sectional Children 8–11 years 303 Drinking water Blood, toenails Motor function (Bruininks-Oseretsky Test) including total score and subscales for coordination of hands and fingers and arms and hands, body coordination, strength and agility
Khan et al. (2012) [58] Araihazar Bangladesh Cross sectional Children 8–11 years 840 Water None measured Academic achievement from nationwide exams in math and language
Wasserman et al. (2011) [30] Araihazar Bangladesh Cross sectional Children ages 8–11 years 299 Well water Blood IQ, (WISC-IV) including verbal comprehension, perceptual reasoning, working memory, processing speed, and full scale scores
Claus Henn et al. (2012) [27] Mexico City, Mexico Prospective Children enrolled prenatally; followed to 36 months 455 None measured Blood Bayley Scales of Infant Development-II (MDI and PDI)
Lucchini, Zoni, et al. (2012) [41] Valamonica and Garda Lake, Italy Cross sectional Children 11–14 years 299 PM10, soil Hair, blood, urine IQ (WISC-III) including the overall, verbal and performance scores), and behavior (Conners-Wells’ Adolescent Self-Report Scale Long Form)
Lucchini, Guazzetti et al. (2012) [33] Valamonica and Garda Lake, Italy Cross sectional Children 11–14 years 54 exposed (157 control) PM10, soil, tap water, diet Hair, Blood Motor coordination (Luria Nebraska Battery) including hand dexterity, odor identification and tremor intensity
Bhang et al. (2013) [40] South Korea Cross-sectional Children 8–11 years 1005 None measured Blood IQ (WASI), ADHD Diagnostic System, Stroop Color-Word Test, Children’s Color Trails Test, ADHD Rating Scale, Learning Disability Evaluation Scale, Child Behavioral Checklist and the Diagnostic Interview Schedule for Children-IV
Torres- Agustín et al. (2013) [54] Hidalgo, Mexico Cross sectional Children 7–11 years 79 (95 control) PM10, soil Hair, Blood Memory and learning (Children’s Auditory Verbal Learning Test) including learning curve and level, immediate and delayed recall, recognition accuracy and immediate memory span
Lin et al.
(2013) [28]
Taipei, Taiwan Prospective Mother-Infant pairs in the Taiwan Birth Panel 230
(pairs)
None
measured
Cord
blood
Development (Comprehensive Developmental Inventory for Infants and Toddlers) global, cognitive, language, motor, gross motor, fine motor, social, self-help, and behavioral development.
Carvalho et al. (2014) [36] Simões-Filho district, Bahia, Brazil Cross
sectional
Children 7–12 years 70 None
measured; participants lived near a ferromanganese alloy plant
Hair IQ (WISC-III), short-term, and working memory, sustained attention problem solving (Wisconsin Card Sorting Test, WCST-64) and sustained attention (TAVIS-III)
Menezes- Filho et al. (2014) [53] Salvador, Bahia, Brazil Cross
sectional
Children 7–12 years 70 None measured, but airborne exposure from residential proximity to ferromanganese plant Hair,
blood
Internalizing and externalizing behaviors, and attention problems (Children’s Behavioral Checklist)
Oulhote et al. (2014) [47] Quebec, Canada Cross
sectional
Children 6–13 years 375 Tap water, water consumption Hair Memory and learning (California Verbal Learning Test-Children’s Version), Connors Continuous Performance Test II, Version 5, Digit Span, Santa Ana Test, manual finger tapping
Rink et al. (2014) [46] Montevideo, Uruguay Cross
sectional
14–45 months old 60 None measured Hair Bayley Scales of Infant Development-III, cognitive, language, fine and gross motor abilities
Yang, et al. (2014) [57] Shangai, China Prospective Mother-infant pairs 933 None measured Cord
blood
Neonatal Behavioral Neurological Assessment
Chung et al. (2015) [42] Seoul, Ulsan and Cheonan, South Korea Prospective Maternal - infant pairs recruited prenatally 232 mother- infant pairs assessed at 6 months postpartum and followed for 3 years None reported Maternal blood Bayley Scales of Infant Development
do Nascimento et al. (2015) [37] Rio Grande do Sul, Brazil Cross
sectional
Children 6–12 years 69 Tap water Hair,
blood
Nonverbal IQ (Raven’s Colored Progressive Matrices)
Gunier et al. (2015) [45] Salinas Valley,
California, US
Prospective Children recruited from prenatal cohort; followed to 7 years 197 (prenatal)
193 (postnatal)
Residential proximity to agricultural use of Mn- containing fungicides and ‘take home’exposures Teeth
(pre- and postnatal dentin from incisors)
Cognitive abilities, fine and gross motor coordination (Bayley’s Scales of Infant Development)
Haynes et al. (2015) [15] Marietta, Ohio, US Cross
sectional
Children 7–9 years 404 None reported; PM2.5 associated with residential proximity to a ferromanganese refinery Hair,
blood
IQ (WISC-IV), including perceptual reasoning, processing speed, working memory and verbal comprehension
Mora et al. (2015) [39] Salinas
Valley,
California,
US
Prospective Children enrolled prenatally provided shed teeth starting at 7–9 years, followed to 10.5 years 248 (prenatal)
244 (postnatal)
Residential proximity to agricultural use of Mn- containing fungicides Teeth
(pre- and postnatal dentin from incisors)
Behavior including internalizing, externalizing and hyperactivity (Behavioral Assessment System for Children; Conners’ Attention Deficit Hyperactivity Disorder; Statistical Manual of Mental Disorders, DSM-IV), accuracy and impulse control (Connors’ Continuous Performance Test II, Version 5)
Cognition and memory including IQ (WISC-IV), verbal comprehension, perceptual reasoning, working memory and processing speed and full-scale score; visuospatial and verbal memory (NEPSY II Memory for Designs) verbal learning and memory abilities (CAVLT-II)
Motor including fine motor dexterity including finger tapping and pegboard at age 7, and subtests of the Luria Nebraska Motor Battery, at ages 9 and 10.5
Ode et al. (2015) [50] Malmö, Sweden Case
control
Children born 1987 to 2000 diagnosed with ADHD 5–17 years; matched controls 166 (case-control pairs) None
measured
Cord
serum
ADHD diagnosis (Diagnostic and Statistical Manual of Mental Disorders, DSMMD-III, IV)
Shin et al. (2015) [51] Seoul,
South
Korea
Case
control
Children, 6–16 years, ADHD cases referred post-diagnosis 40 cases (43 controls) None
measured
Hair ADHD diagnosis
DSMMD- IV, Kiddie-Schedule for Affective Disorders and Schizophrenia-Present and Lifetime Version and other tests
Sun et al. (2015) [38] Jiangsu,
China
Cross
sectional
Children, 8–12 years with natural environmental lead exposure 446 Mean community Pb concentrations in surface soil: 27.7 mg/kg, -1 and undetected levels in outdoor air (<0.0035 mg/ m-3 Blood IQ (Combined Raven Test
modified in China)