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Table 1 Summary of the articles using resting and functional/cognitive TCD measures to investigate the association between blood flow velocity and cognition in children

From: Cerebrovascular function and cognition in childhood: a systematic review of transcranial doppler studies

Article

Participants v controls (if applicable)

Total N (subgroups)/mean age (sd)/% males

TCD protocol and vessel(s)

Cognitive measure

Relevant findings

RESTING TCD STUDIES

    

In infants

    

Rennie et al. [13]

Low birth weight infants with developmental delay (DD) v normal development infants

n = 74 (DD n = 9, control n = 42)/mean gestational age weeks DD 27 (SD = 1), control 29 (SD = 2)/DD 67% male, control 50% male

Resting TCD; MV recorded over first 3 days of life

BSID (mental development) taken at 18 months of age.

DD infants less likely to show the usual steady increase in SV. A larger percentage (44%) of DD infants displayed a rise, then a fall, in CBFV compared to infants in the control group (13%).

Unilateral ACA

Ojala et al. [12]

Ventilated preterm infants with RDS (V-RDS) and non-ventilated preterm infants with no signs of RDS (N-RDS)

n = 49 (V-RDS n = 35, N-RDS n = 14)/V-RDS mean gestational age 29 weeks (SD = 1), N-RDS mean gestational age 31 weeks (SD = 1)/V-RDS 57% males, N-RDS 57% male

Resting TCD; SV, DV, MV and RI taken at 6, 12, and 24 hours post-birth

10-min Apgar score.

In N-RDS group, lower RI was associated with poorer neurologic results at 12 months. No association in V-RDS group.

GMDS (physical and mental development) at 12 months.

Unilateral ACA

Arditi et al. [11]

Premature infants

n = 51/mean gestational age weeks 30 (SD = 3)/53% male

Resting TCD; SV, DV and MV

NBAS (visual/auditory habituation) at 37 weeks gestational age.

Greater right SV related to lower neonatal performance on the NBAS. Greater left SV related to high MDI scores at 24 months. Left > right SV related to better neonatal orientation and high MDI scores at 24 months.

Bilateral MCA

BSID-II (mental development) at 6, 12, and 24 months.

Scherjon et al. [14]

Premature infants

n = 123/mean gestational age 31 weeks/sex not reported

Resting TCD; MV and MV ratio (defined as MV during the first 12 hours after birth, divided by mean velocity in the period 12-hours post-birth)

Prechtl score (neurological functioning) at 40 weeks corrected gestational age.

Prechtl scores were related to MV ratio – high Prechtl score related to low MV ratio (reflecting MV not increasing over first days of life). No relationships between Touwen scores and TCD measures.

Touwen score (neurological functioning) at ages 6 and 12 months.

MCA

Alatas et al. [15]

Infants from HRP mothers v infants from normal pregnancy mothers

n = 237 (HRP n = 75, control n = 162)/mean gestational age at delivery HRP 38 weeks, control 39 weeks/sex not reported

In-utero from 24 weeks gestation until delivery

1 and 5-minute Apgar scores (general and neurological functioning).

Positive relationship between MCA PI and 5-min Apgar scores in infants from HRP; no relationship in control group.

MCA

In Sickle Cell Disease

    

Hogan et al. [19]

Infants with SCD v healthy infants

n = 28 (SCD n = 14, control n = 12)/between 1-13 months/SCD 79% male, control 42% male

Resting TCD; SV and MV recorded at ages 3, 9 and 12 months

BINS (neurological function) taken at 3, 9 and 12 months.

Infants with SCD had increased SV and MV, which were associated with a higher risk of neurodevelopmental delay at 9 months of age (not 3 or 12 months).

BA, bilateral MCA and ICA

Armstrong et al. [30]

Infants with SCD

n = 208/mean age 13 months (SD = 3)/43% male

Resting TCD; SV

BSID-II (mental, motor and behavioural development), VABS (developmental status based on parent report).

Lower VABS scores (communications, daily living skills and socialisation domains) were associated with greater SV. No association between SV and BSID-II.

Vessel not specified

Schatz et al. [25]

Children with SCD

n = 50/mean age 26 months (SD = 13)/56% male

Resting TCD; MV

DDST-II (infant and childhood development).

Children with developmental delays had significantly higher MCA MVs, compared typically developing children (all with SCD).

Bilateral ICA and MCA

Note: TCD in an n = 30 subsample

VABS (developmental status based on parent report)

Aygun et al. [16]

Children with SCD

n = 88/mean age 4 years (SD < 1)/51% male

Resting TCD; MV

BPS-II (motor, language and cognitive development).

No association was found between TCD measures and cognitive performance.

BA, bilateral MCA, ACA, PCA and ICA

Sanchez et al. [24]

Children with SCD

n = 39/mean age 6 years (SD = 1)/41% male

Resting TCD; SV

TOLD-P:3 (language ability).

Higher SVs were associated with poorer syntactical ability.

Bilateral MCA

WJ-III (academic achievement).

Strouse et al. [26]

Children with SCD

n = 24/mean age 9 years (SD = 2)/sex not reported

Resting TCD; SV

WASI (IQ).

No significant correlation between SV and IQ.

Bilateral ACA

Onofri et al. [31]

Children with SCD

n = 35/mean age 9 years (SD = 3)/49% male

Resting TCD; SV

WISC-II (IQ) for children aged 6-16 years.

There were no differences between mentally impaired and non-impaired groups in those terms of percentage with abnormal SV.

Abnormal SV defined as >170 cm/s

Vessel unspecified

WPPSI-III (IQ) for children aged 4-6 years.

Kral et al. [22]

Children with SCD

n = 60/mean age 121 months (SD = 31)/43% male

Resting TCD; SV

WASI (IQ).

Children with abnormal TCD had lower verbal IQs than children with conditional TCD. Children with conditional TCD performed worse than children with normal TCD on measures of executive function. The conditional TCD group was slowest to complete the TMT.

Abnormal TCD defined as SV > 200 cm/sec; conditional TCD defined as SV = 170-200 cm/sec; normal TCD defined as SV <170 cm/sec

WJ-R (academic achievement).

CPT-II (visual sustained attention).

CMS (working memory).

Bilateral MCA and ICA

TMT (visual attention).

BRIEF (executive functioning).

Kral and Brown [20]

Children with SCD

n = 62/mean age 121 months (SD = 31)/43% male

Resting TCD; MV

Academic attainment; grade retention and special education placement.

Children with abnormal TCD received significantly more special education services.

Abnormal TCD defined as SV > 200 cm/sec

Bilateral MCA and ICA

Kral et al. [21]

Children with SCD

n = 27/mean age 129 months (SD = 36)/44% male

Resting TCD; MV

WASI (IQ).

When controlled for age and hematocrit, children with abnormal TCD had better verbal memory in comparison to children with normal TCD.

Abnormal TCD defined as SV > 200 cm/sec; normal TCD defined as SV < 170 cm/sec

WJ-R (academic achievement).

CPT-II (sustained attention),

Bilateral MCA, ACA and ICA

CMS (working memory).

TMT (visual attention).

Academic attainment; grade retention and special education placement.

DTVMI (visuo-motor integration).

Hijmans et al. [18]

Children with severe SCD

n = 37/mean age 12 years (SD = 3)/53% male

Resting TCD; MV (within 14 months preceding neurocognitive testing)

WISC-III/WAIS-III (IQ),

No associations between TCD and cognitive measures. However, sustained attention better in children with right > left resting MV.

Stop task (response inhibition and sustained attention), Tower of London (planning),

Bilateral MCA, ACA and ICA

N-back task; (working memory).

Bernaudin et al. [17]

Children with SCD v siblings without SCD

n = 249 (SCD n = 173, control n = 76)/mean age SCD 10 years (SD = 3), not reported for controls/SCD 51% male, controls not reported

Resting TCD; SV, DV and MV

WISC-II/WPPSI-R (IQ).

SCD sample: children with abnormal TCD had lower IQ scores (picture arrangement and performance IQ).

Abnormal TCD defined as SV > 200 cm/sec

BA, bilateral MCA, ACA, PCA, and ICA

Effect did not hold after excluding those with stroke.

TCD only collected on a n = 143 subsample

Ruffieux et al. [23]

Children with SCD

n = 32/between 6 and 24 years of age/48% male

Resting TCD; SV and DV

CVLT (memory). Executive function/attention tasks including

Children with A-TCD had worse memory performance, as compared to children with N-TCD measurements.

Normal (N-TCD) defined as max. velocity <170 cm/sec; abnormal (A-TCD) defined as max. velocity >200 cm/sec or peak systolic ≥ 250 cm/sec

Colour trails, digit span, coding, verbal semantic fluency test, bell cancellation task, letter-number sequencing and CPT.

OA, MCA, ACA, BA, ICA

 

In sleep disordered breathing

    

Hill et al. [17]

Children with mild SDB v healthy control children

n = 31 (SDB n = 21, control n = 17)/mean age SBD 6 years (SD = 1), control 5 years (SD = 1)/SDB 43% male, control 53% male

Resting TCD; SV, MV

WPPSI-III (IQ).

CBFV significantly increased in the SDB group, as compared to controls. SDB children achieved lower scores on processing speed and visual attention, but no direct association with CBFV.

Bilateral MCA

NEPSY (neuropsychological development).

BRIEF (executive functioning).

FTCD STUDIES

    

In clinical groups

    

Bruneau et al. [27]

Children with autistic behaviour (AB), mentally retarded children without autistic symptoms (MR) and healthy control children

n = 34 (AB n = 12, MR n = 10, control n = 12)/mean age AB 7 years (SD = <1), MR 6 years (SD < 1), control 7 years (SD < 1)/AB 67%, MR 70%, control 33% male

fTCD using auditory stimuli (passive task); SV, DV, MV and RI

Auditory tone stimuli

Auditory stimulation increased velocities and decreased RI on the left side for the control children. Same pattern for MR children, but less asymmetrical. AB children displayed a symmetric and opposite pattern, with velocities decreasing and RI increasing on both sides.

Bilateral MCA

In typically developing children

    

Stroobant et al. [32]

Typically developing children

n = 26/mean age 82 months/46% male

fTCD using visual stimuli requiring expressive response, and auditory stimuli requiring no response; MV and calculated LI (left-right MV in response to stimuli)

Taaltest voor kinderen/“language tests for children” (language development)

The expressive language task elicited a stronger left LI than the passive language task. Good test-retest reliability for TCD. No relationship between LI and Dutch language test.

Bilateral MCA

Lohmann et al. [4]

Typically developing children

n = 10/2-10 years of age/40% male

fTCD with a picture description task; MV and calculating LI (left-right MV in response to stimuli)

Illinois Test of Psycholinguistic

Left lateralised increased in blood flow velocity (i.e. positive lateralisation index), however this did not relate to language ability.

Abilities

Bilateral MCA

Groen et al. [2]

Typically developing children

n = 14/mean age 7 years (SD < 1)/57% male

fTCD using visual stimuli requiring a physical response; MV and calculated LI (left-right MV in response to stimuli)

Rabbits paradigm (visuospatial memory)

A negative LI was found, indicating right lateralisation. Task performance unrelated to LI.

Bilateral MCA

Groen et al. [3]

Typically developing children

n = 60/6-16 years of age/43% male

fTCD using visual stimuli requiring a verbal and physical response; MV and calculated LI (left-right MV in response to stimuli)

LIPS-R (performance IQ).

Most children (58%) were left lateralised for language, and right lateralised for visuospatial memory. Children with left lateralisation language had better vocabulary and non-word reading performance (independent of laterality of visuospatial memory).

BPVS-2 (receptive vocabulary).

TOWRE (reading). NEPSY (phonological short-term memory).

Bilateral MCA

Haag et al. [28]

Typically developing right handed children

n = 45 (children n = 23, adolescents n = 22)/mean age children 8 years (SD = 2), adolescents 15 years (SD = 2)/children 48% males, adolescents 36% males

fTCD using visual stimuli requiring a verbal response; MV and calculated LI (left-right MV in response to stimuli)

Visual stimuli.

The world generation task (adolescents only) produced left lateralised response, but this was not the case for the picture description task, regardless age group.

Children completed a non-lexical picture description task. Adolescents additionally completed a lexical word generation task

Bilateral MCA

  1. Vessels: ACA Anterior cerebral artery, BA Basilar artery, ICA Internal cerebral artery, MCA Middle cerebral artery, OA Ophthalmic artery, PCA Posterior cerebral artery, RCP Regional cerebral perfusion.
  2. Health Conditions: HRP High risk pregnancy, RDS Respiratory distress syndrome, SCD Sickle cell disease, SDB Sleep disordered breathing, HLHS Hypoplastic left heart syndrome.
  3. Neurocognitive Measures: NBAS Neonatal Behaviour Assessment Scales. BINS Bayleys Infant Neurodevelopmental Screener, BSID Bayley Scales of Infant Development, BSID-II Bayley Scales of Infant Development-II, BSITD-III Bayleys Scales of Infant and Toddler Development-III, BRIEF Behaviour Rating Inventory of Executive Functioning, BPS-II Brigance Preschool Screen-II, BPVS-II British Picture Vocabulary Scale-II, CVLT California Verbal Learning Test for Children, CMS Children's Memory Scale, CPT/CPT-II Conners's Continuous Performance Test-II, DDST-II Denver Developmental Screening Test, GMDS Griffith’s Mental Development Scale, LIPS-R Leiter International Performance Scale-Revised, NEPSY Neuropsychological Test Battery for Children, TOLD-P:3 Test of Language Development-Primary Third Edition, TOWRE Test of Word Reading Efficiency, TMT Trail Making Test, WASI Wechsler Abbreviated Scale of Intelligence, WAIS-III Wechsler Adult Intelligence Scale-III, WISC-II/WISC-III Wechsler Intelligence Scale for Children, WPPSI-III/WPPSI-R Wechsler Preschool and Primary Scale of Intelligence, WJ-R/WJR-III Woodcock-Johnson Psycho-Educational Battery, VABS Vineland Adaptive Behaviour Scales.