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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)