We describe six psychomotor, language, and neuropsychological sequential developmental evaluations in a boy who sustained a severe bifrontal traumatic brain injury (TBI) at 19 months of age. Visuospatial, drawing, and writing skills failed to develop normally. Gradually increasing difficulties were noted in language leading to reading and spontaneous speech difficulties. The last two evaluations showed executive deficits in inhibition, flexibility, and working memory. Those executive abnormalities seemed to be involved in the other impairments. In conclusion, early frontal brain injury disorganizes the development of cognitive functions, and interactions exist between executive function and other cognitive functions during development.
Traumatic brain injury (TBI) sustained at a very young age is associated with high rates of long-term morbidity and mortality. The aetiology and pathophysiology of head injuries in children younger than 4 years of age differ from those in older children. Although the causes of TBI in children under 4 include falls, as well as traffic accidents as passengers [
The first postnatal years are characterized by an extremely fast rate of brain growth, which involves numerous processes such as dendritogenesis, axogenesis, synaptogenesis and synaptic stabilisation, gliogenesis, and myelination [
Differences in outcomes according to which cerebral lobe is involved, and more specifically the impact of frontal lobe damage, have been investigated in several series of school-aged children. Several studies assessed the influence of frontal lobe involvement on cognitive functions, including intellectual and executive functions [
Little is known about the impact of frontal lobe involvement on outcomes after TBI in very young children. A single case-series of children with frontal lobe injury included patients younger than 6 years at injury [
A number of case-reports have supplied information on adulthood outcomes after frontal lobe injury sustained in early childhood [
Here, we report on a patient who sustained bilateral frontal lobe damage at 19 months of age during a domestic accident and who was subsequently evaluated six times between the ages of 3 years 9 months and 9 years 10 months. The development of psychomotor, language, and executive functions in this patient is described below.
The patient was a boy born to Moroccan parents living in the French-speaking part of Belgium. Delivery was normal. He learned to walk at 13 months. Both French and Arabic were spoken at home, and his language development was normal.
At 19 months of age, he fell from a height of six meters. He did not lose consciousness. He was taken immediately to the emergency room, where the physical examination showed a deep wound in the forehead, bilateral epistaxis, periorbital hematoma, and palpebral oedema. He was irritable and a language deficit was noted. His deep tendon reflexes and plantar reflexes were normal but he had mild paresis of the left lower limb. Computed tomography (CT) of the brain showed multiple fractures of the frontal bone with displaced fragments; fractures of the ethmoidal bone, right supraorbital area, and right nasal bone; and brain oedema. Surgery of the displaced frontal bone fracture was performed 2 days after the fall. The postoperative course was favourable, with gradual improvement of the paresis of the left lower limb. Two weeks later, magnetic resonance imaging (MRI) disclosed bilateral high signal from the base of the frontal cortex, as well as a right anterior insular lesion. Two years later, a control MRI showed stability in white matter lesions, but atrophy of bifrontal cortex was more severe (Figures
Magnetic Resonance Imaging (MRI) performed 2 weeks after trauma: FFE-coronal (a), T1 weighed (b), and T2-axial (c) sections showed bilateral (right
A control MRI was performed 2 years after trauma: FLAIR section (a) showed stable white matter lesions (right fronto-parietal and left posterior-parietal), T2-weighed (b) and T1-axial (c) sections showed worsening in bi-frontal atrophy.
He was first evaluated at our clinical unit when he was 3 years 9 months old. Subsequently, we re-evaluated him once a year, for a total of six evaluations; thus, at the last evaluation, he was 9 years 10 months old. His cognitive development was assessed using measures of motor function, language, and neuropsychological status.
His parents were attentive observers, who noticed changes over the years. Immediately after the injury, they detected no behavioural or emotional changes, except regarding language. However, 2 months later, his parents described him as “hyperactive” at home, moving around continuously and unable to remain still or to play the same game for more than a few minutes.
He started to attend nursery school 18 months after the injury, when he demonstrated difficulties relating to his peers. He spoke only about five words and was extremely restless. Psychomotor disturbances emerged at that time: thus, although he was then 3 years old he was unable to distinguish a circle from a square, to pedal on a tricycle, or to put his finger on his mouth or nose. Consequently, psychomotor and speech rehabilitation therapy was started. About 6 months later (when he was 3 years 6 months, 2 years after the injury), he had attentional deficits, delayed language development with a combination of vocabulary deficiency and receptive language impairment, and delayed motor development. He experienced considerable difficulty relating to other children. French was chosen as his main language, as bilingualism was felt to be too complicated for him.
Three years after the injury (when he was 4 years 10 months old), he was less hyperactive but exhibited major attention deficiency, particularly in his class group, where he was easily distractible and seemed not to hear others. One year later (when he was 5 years 9 months old, 4 years after the injury), he was described as very impulsive, with deficits in expressive language and in psychomotor skills. He therefore repeated his third year of nursery school. When he was 7 years old, his persistent difficulties with attention and language led to his enrolment in a special-education program.
During the last two evaluations at our clinical unit, he seemed excessively obedient and polite: for example, he did not ask for food when he was hungry. On the other hand, he occasionally exhibited symptoms of hyperactivity, running and jumping during games that did not require physical activity. At school, he was described as the perfect student, being interested in everything, very polite, and reserved. His parents, however, reported difficulty concentrating on his homework. The last evaluation was performed when the parents asked that he be returned to the mainstream school system, as they felt he no longer required special education. No parental scales were used to confirm these observations of family.
Cognitive development was assessed using measures of (a) general intellectual abilities, (b) attentional and executive functions, (c) working memory, (d) language, and (e) psychomotor skills.
We chose among the following scales based on age at evaluation: Wechsler Intelligence Scale for Pre-school Children—Revised [
Few tools are available for measuring these functions in young children. An increasing number of tests were performed from one evaluation to the next, as the patient advanced in age.
The following tests were used. Crossing tasks from the NEPSY [ The visual selective attention task on the TAP (Test Battery for Attentional Performance [
A dual task from the TAP [
The 10-minute Zazzo Cancellation Task was used. The child is asked to cross out as fast as possible two kinds of target signs on sheets that also contain distractor signs, for 10 minutes. Time to completion and accuracy are recorded.
Both cognitive and behavioural inhibitions were measured, using the tests listed below. Statue test from the NEPSY [ Knock-and-tap test from the NEPSY [ Go/No-Go task from the TAP [ The Interference Fruit Task [ Incompatibility (TAP [
Spontaneous and reactive flexibility [
The Tower of London test was used. Number of models built successfully at the first attempt, total number of trials needed to build the 12 models, planning times, and execution times were recorded.
Both verbal and visuospatial tasks requiring working memory were evaluated. The verbal tasks focused on the temporary retention of words or numbers. The visuospatial tasks assessed the temporary retention of sequential or simultaneous images. Working-memory tests included the hand movements and spatial memory tasks from the KABC scale [
It was evaluated using the praxis tests from the BEPL [ We used the MSCA subtest [ We used a test from the L2MA [ We used the BEPL phonology subtests (PHO1 & PHO2 [ We used the “VOC” subtest from the NEEL [ We first used the BEPL [ Two tests were used: the TCG [
We used the GNO subtest from the BEPL [ The TVAP 3–5 and 5–8-year test [ It was evaluated only after 6 years of age, using the O-52 [ They were used until the patient was 6 years of age. These scales assess both receptive and expressive language in children between 1 and 6 years of age. When the patient was 8 years old, we used three subtests from the BELEC [
Psychomotor development was assessed using the Oseretsky Test [
The test scores are recapitulated in Table
Intellectual evaluations (Wechsler scales).
4 years 10 months | 5 years 9 months | 6 years 7 months | 8 years 3 months | 9 years 8 months | |
WPPSI-R | WPPSI-R | WISC-III | WISC-III | WISC-IV | |
Verbal IQ (or verbal comprehension for WISC-IV) | 69 | 76 | 71 | 80 | 84 |
Performance IQ (or perceptual reasoning for WISC-IV) | 76 | 84 | 76 | 73 | 77 |
Full-scale IQ | 72 | 78 | 69 | 73 | 73 |
Intellectual evaluation. VIQ: verbal intellectual quotient; PIQ: performance intellectual quotient; TIQ: full-scale intellectual quotient.
The first two evaluations performed at 3 years 9 months and 4 years 10 months were somewhat crude given the young age of the patient. The results indicated a deficiency in visual selective attention during NEPSY tasks (bunnies and cats crossing task).
Subsequent assessments were more sophisticated. They were performed at 6 years 7 months, 8 years 3 months, and 9 years 8 months of age (see Table
Attentional evaluations.
6 years 7 months | 8 years 3 months | 9 years 8 months | ||||
Z Score | Raw Score | Z Score | Raw Score | Z Score | Raw Score | |
Cats crossing (NEPSY) | ||||||
Times (sec.) | +0.1 | 63 | +0.6 | 35 | +0.3 | 39 |
Omissions | 1 | 1 | +0.4 | 0 | ||
Commissions | +0.1 | 0 | +0.1 | 0 | +0.2 | 0 |
Faces crossing (NEPSY) | ||||||
Times (sec.) | 180 | 140 | +0.7 | 107 | ||
Omissions | +0.4 | 4 | 7 | 8 | ||
Commissions | 15 | 12 | 4 | |||
Visual attention task (TAP) | ||||||
Mean reaction times | +2.3 | 879 | 1274 | 1255 | ||
Omissions | +1.9 | 4 | 9 | 5 | ||
Commissions | 32 | 7 | +0.8 | 0 | ||
10-minute Zazzo | ||||||
Speed | — | — | 360 | 439 | ||
Accuracy | — | — | 41.5 | 14.5 | ||
Divided Attention Task (TAP) | ||||||
Reaction times (msec.) | — | — | 975 | 946 | ||
Omissions | — | — | 13 | 8 | ||
Commissions | — | — | +0.4 | 1 | +0.9 | 0 |
The first evaluations consisted only in the NEPSY statue test, given the young age of the patient (3 years 9 months, 4 years 10 months, and 5 years 9 months). Although the parents reported hyperactivity, the results of the first two evaluations was within the normal range. The third evaluation supported the parents’ report of restlessness, as the raw score remained unchanged, at 11. However, a more sophisticated evaluation 1 year later (at 6 years 7 months of age) was within the normal range, with no restlessness, despite reports of inattention at home and at school.
Difficulty with inhibition was noted at the last two evaluations performed when the patient was 8 years 3 months and 9 years 8 months of age (see Table
Executive function evaluations.
6 years 7 months | 8 years 3 months | 9 years 8 months | ||||
Percentile | Raw score | Percentile | Raw score | Percentile | Raw score | |
Statue (NEPSY) | 26–75 | 25 | 11–25 | 25 | 26–75 | 27 |
Knock and Tap (NEPSY) | 26–75 | 27 | 11–25 | 22 | 26–75 | 29 |
Go/No-Go (TAP) | ||||||
Median reaction times (msec.) | — | — | 97 | 358 | 88 | 404 |
Omissions | — | — | 3 | 4 | 3 | 4 |
Commissions | — | — | 3 | 9 | 4 | 8 |
Go/No-Go (KITAP) | ||||||
Median Reaction Times (msec.) | — | — | 331 | 66 | 442 | |
Omissions | — | — | 10 | 2 | 42 | 3 |
Commissions | — | — | 5 | 7 | >34 | 0 |
Incompatibility (TAP) | ||||||
Median reaction times (msec.) | — | — | — | — | 98 | 338 |
Commissions | — | — | — | — | <1 | 31 |
Z score | Raw score | Z Score | Raw Score | Z Score | Raw Score | |
Fruit Stroop Task | ||||||
Naming times (sec.) | 65 | 36 | 35 | |||
Naming errors | 2 | 2 | 2 | |||
Interference times (sec.) | 97 | 82 | 83 | |||
Interference errors | 4 | 7 | 8 | |||
Flexibility Task (TAP) | ||||||
Mean reaction time (msec.) | 2694 | 1570 | +0.03 | 1363 | ||
Hits | 39 | 30 | 42 | |||
Errors | 11 | 15 | 8 | |||
Verbal fluency (NEPSY) | ||||||
Animal | +0.3 | 11 | +0.9 | 15 | +1.3 | 19 |
Beverages and foods | 4 | 12 | 11 | |||
Design fluency (NEPSY) | ||||||
Structured array | 4 | +0.1 | 11 | +0.4 | 13 | |
Random array | 5 | 9 | 12 | |||
Tower of London | ||||||
First trials | — | — | +0.6 | 7 | +2.0 | 9 |
Total trials | — | — | +0.9 | 19 | +2.1 | 15 |
Planning times (sec.) | — | — | +0.8 | 4.5 | 7.4 | |
Execution times (sec.) | — | — | +0.3 | 5.6 | 8 |
Planning and organization were within the normal range at 8 years 3 months of age. The last evaluation (9 years 8 months) showed excessively long planning and execution times on the Tower of London test, although the quality of the response was very good, suggesting that the patient took care to comply with the instruction to make as few mistakes as possible.
The serial evaluations showed no progress in working memory for those tests where there is no learning effect (Digit span, Block Tapping Test). Tests from the K.ABC were impaired at the first evaluation and became normal subsequently (see Table
Working memory evaluations.
4 years 10 months | 5 years 9 months | 6 years 7 month | 8 years 3 months | 9 years 8 months | ||||||
Z-score | Raw score | Z-score | Raw score | Z-score | Raw score | Z-score | Raw score | Z-score | Raw score | |
Digit span | 2 | 3 | 3 | 3 | 3 | |||||
Reverse digit span | — | — | — | — | 2 | 3 | ||||
Word set (K.ABC) | 3 | 5 | 6 | 6 | — | — | ||||
Block Tapping Test | 3 | 2 | 2 | 3 | — | — | ||||
Hand movements (K.ABC) | 5 | 8 | +0.3 | 11 | 5 | — | — | |||
Spatial memory (K.ABC) | — | — | 8 | 9 | 8 | — | — |
Time-course of verbal and visual spans in working memory.
Motor quotients were consistent with the total IQs from the general intellectual evaluations (see Figure
Psychomotor evaluations.
3 years 9 months | 4 years 10 months | 5 years 9 months | 8 years 3 months | 9 years 8 months | |
---|---|---|---|---|---|
Basis age | 2 years | 3 years | 3 years | 4 years | 4 years |
Motor age | 2.8 years | 3.6 years | 4.4 years | 5.10 years | 6.8 years |
Motor quotient | 73 | 74 | 76 | 71 | 70 |
Time-course of the motor quotient from the Oseretsky test and total IQ from the intellectual evaluation (both tests have an average of 100 and a standard deviation of 15 in the general population).
At the first evaluation, praxis performance and auditory processing were within the normal range; whereas deficiencies were noted in phonology, morphosyntax, and lexical processing (during both expression and comprehension). Praxis remained good at the following evaluations.
The evaluations of expressive language showed weaknesses or deficiencies in phonology until 8 years of age (see Tables
Language assessments from 3 to 5 years of age.
3 years 9 months | 4 years 10 months | 5 years 9 months | ||||
Percentile | Raw Score | Percentile | Raw Score | Percentile | Raw Score | |
Praxis: BEPL (Pra) | 85 | 93.3% | 50 | 86.7% | — | — |
Semantic fluency: Mc Carthy | — | — | — | — | 33 | 13 words |
Phonology | ||||||
BEPL PHO1 | 12 | 61% | 11 | 79% | <1 | 73.6% |
BEPL PHO2 | 7 | 50.6% | 15 | 77% | <1 | 69.5% |
Repetition | ||||||
Syllables | ||||||
BEPL Art 1 | 1-2 | 62.5% | 9* | 75% | 1* | 62.5% |
BEPL Art 2 | — | — | 23* | 73.3% | 5* | 60% |
Sentences | ||||||
BEPL RPH1 | — | — | 16* | 20/26 | 60* | 24/26 |
BEPL RPH2 | — | — | 5* | 24/40 | 35* | 31/40 |
Morphosyntax | ||||||
TCG | 4/52 | 2 | 14/52 | <1 | 19/52 | |
TVAP definitions | — | — | 3 | 13/60 | — | — |
Auditory discrimination | ||||||
BEPL Gno | 45 | 50% | 82 | 100% | — | — |
TVAP 3–5 | 18/60 | 6 | 41/60 | 25 | 50/60 | |
EVIP (Peabody) | 3 | 8/170 | — | — | ||
Reynell | Developmental age | Developmental age | Developmental age | |||
3 years | 39 | 3,11 years | 50 | 5 years | 59 |
Language assessments from 6 to 9 years of age.
6 years 7 months | 8 years 3 months | 9 years 6 months | ||||
Percentile | Raw Score | Percentile | Raw Score | Percentile | Raw Score | |
Praxia: HENIN | — | — | 50 | 46/62 | — | — |
Semantic Fluency: Mc Carthy | 79 | 21 words | 73 | 27 words | 50 | 20 words |
Phonemic Fluency: L2MA | — | — | 4 | 6 words | 50 | 13 words |
Vocabulary | ||||||
EEL LX2/NEEL voc 1 | 19% | 4 | 47/72 | 68 | 64/72 | |
EEL LX3/NEEL voc 2 | 1 | 29% | 5 | 32/42 | 33 | 36/42 |
L2MA | — | — | 10 | 9/25 | 23 | 13/25 |
Phonology | ||||||
EEL Dex | 11 | 90.3% | — | — | — | — |
NEEL monosyllabic words | — | — | 24/28 | 62 | 28/28 | |
NEEL polysyllabic words | — | — | 44/50 | 61 | 50/50 | |
Repetition | ||||||
Words | ||||||
EEL Rep | 84.8% | — | — | — | ||
NEEL monosyllabic words | — | — | 26/28 | 57 | 28/28 | |
NEEL polysyllabic words | — | — | 54 | 50/50 | 54 | 50/50 |
Sentences | ||||||
EEL PH1 | 16 | 50% | — | — | — | — |
EEL PH2 | 4 | 60% | — | — | — | — |
NEEL B1 Syntax | — | — | 0/2 | 64 | 2/2 | |
NEEL B1 Numbers of words | — | — | 19/31 | 9 | 24/31 | |
NEEL B2 Syntax | — | — | 50 | 0/1 | 54 | 1/1 |
NEEL B2 Numbers of words | — | — | 19 | 13/25 | 41 | 17/25 |
Non words | ||||||
BELEC CV | 15 | 13/20 | 38 | 15/20 | 50 | 16/20 |
BELEC CV Span (syllables) | 51 | 5 | 58 | 5 | 58 | 5 |
BELEC CCV | — | — | 37 | 9/20 | 47 | 10/20 |
BELEC CCV Span (syllables) | — | — | 37 | 3 | 30 | 3 |
Morphosyntax | ||||||
TCG | 3 | 23/52 | 5 | 32/52 | 5 | 38/52 |
TVAP definitions | 16 | 29/60 | 2 | 25/60 | 37 | 40/60 |
Auditory discrimination | ||||||
Words | ||||||
EDP 4–8 | 32/32 | 32/32 | >80 | 32/32 | ||
TVAP 5–8 | 35 | 52/60 | 16 | 47/60 | 63 | 55/60 |
EVIP (Peabody) | 25 | 57/170 | 45 | 80/170 | 60 | 105/170 |
Sentences | ||||||
O52 (Khomsi) | 50 | 46/52 | 50 | 49/52 | — | — |
ECOSSE | 17 | 22 errors | 20 | 12 errors | 6 | 14 errors |
Syllabic reversal (BELEC) | — | — | 90 | 10/10 | 90 | 10/10 |
Phonemic reversal (BELEC) | — | — | 3 | 5/10 | 90 | 10/10 |
Consonant subtraction (BELEC) | — | — | 0/10 | 50 | 9/10 |
Receptive language skills were consistently better than expressive skills. At the last evaluation, receptive language was nearly normal. Auditory discrimination remained excellent. Passive vocabulary was deficient at the first evaluation and slightly improved but nevertheless weak at the second evaluation; it developed favourably starting at 5 years of age and was within the normal range at the last evaluation. Syntactic comprehension was tested after the patient reached 6 years of age; the results were within the normal range until 8 years of age and weak at the last evaluation 1 year later.
Metaphonological skills, necessary for learning written language, were investigated only at the last two evaluations (see Table
Overall, whereas most language test results were weak or deficient at the first evaluation, all language skills except morphosyntax were within the normal range at the last evaluation. Thus, the patient’s oral-language performance was good at last followup, except regarding morphosyntax. Moreover, he experienced major difficulties with written language: thus, at 8 years of age he was able to recognize only about 20 letters and to read consonant-vowel syllables made up of those letters. He confused letters that have similar shapes. His writing skills were weak. At last followup, his academic skills were at the level of the second grade of primary school.
This paper reports on the prospective 8-year followup, including repeated motor and cognitive testing, of a patient who sustained a bifrontal brain injury at 19 months of age. To our knowledge, this is the first such case report. Although clinical and ecological observations showed steady improvement, severe impairments persisted in important areas such as the IQ, psychomotor skills, and executive functions. Moreover, executive function performance worsened over time.
Previous reports described either adulthood outcomes after bifrontal injury in childhood or childhood outcomes after unilateral frontal injury. Price et al. [
Because all these patients were examined as adults, the relation between the early frontal damage and the cognitive or behavioural deficits remained unclear. A few prospective case studies were reported more recently. In 1992, Marlowe described how a small injury to the right frontal lobe sustained at 3 years of age disrupted the acquisition of executive and emotional control over the next 3 years, interfering with the development of adaptive behaviours, executive control, emotional regulation, and personality [
Intellectual stagnation over time is of major concern. We recently reported alarming data about the intellectual development of children after severe brain injury in early life [
During the 8-year followup after the injury, our patient received one-on-one motor and speech rehabilitation therapy. However, improvements in motor function were slow, and impairments in visuospatial functions and graphic skills persisted. Over time, his intellectual and motor quotients remained within the same range.
The language assessments produced interesting data in our patient. Most areas were impaired at the first evaluation, including phonology, morphosyntax, and lexical processing, for both expressive and receptive language. At the last evaluation, in contrast, only morphosyntax remained deficient. The morphosyntax deficiency may be ascribable to a working memory deficit, as morphosyntax tests involve the manipulation of verbal information. He continued to experience major difficulties with written language: at 8 years of age, he could recognize only 20 letters and read only consonant-vowel syllables made up of those letters; in addition, he confused letters of similar shape. These last difficulties may be ascribable to the deficiency in visual selective attention, corresponding to a more basic deficit [
Tests for attention showed a persistent deficit in visual selective attention, which was not addressed by remedial therapy. The last two evaluations showed the emergence of difficulties with inhibition. In contrast, symptoms indicating deficient inhibition (e.g., distractibility and restlessness) were reported from the beginning, and some of them resolved over the years. Flexibility was impaired at the next-to-last evaluation but normal at the last evaluation, although clinical observation continued to show perseverative behaviours. The emergence of executive difficulties during the evaluations was consistently delayed compared to the behavioural observations: thus, the test abnormalities did not coincide with the difficulties reported in everyday life. In addition, some abnormalities resolved from one evaluation to the next yet remained present upon clinical observation. These data raise questions about test sensitivity, their ecological relevance, and the possible impact of learning effects. Impairments in planning and organisation were detected only at the last evaluation, whereas several WISC-III subtests (e.g., picture arrangement, described as sensitive to frontal damage and disordered executive function by Van der Linden et al. [
We consider that clinical attentional or executive deficits result from early damage of anatomo-functional frontal system, but language, psycho-motor, and visuospatial skills may result from interaction with executive functioning or directly from more diffuse lesions.
Repeated evaluations of working memory showed no progress in storage capacities for tests that are not susceptible to learning effects (digit span and block tapping test). At the last evaluation, storage in the phonological loop and visuospatial pad tests was deficient overall. Remedial treatment for the attentional and executive impairments was not given, for practical reasons.
Regarding behaviour, our patient is the first to be described as exhibiting hyperactivity and difficulties with social integration. Over the years, his hyperactivity decreased, and at last follow-up he was almost too quiet and polite. He experienced persistent difficulties in relationships with his peers, as a result of his interests being appropriate for a younger age group and of his reserved behaviour.
Enrolment in a special-education program became necessary when he was 7 years of age. The program allowed him to substantially improve his language skills. The school evaluations showed evidence of learning, albeit at a slower pace compared to other children. Thus, at last followup, he was 2 grades behind in French and arithmetic, although he had none of the typical signs of dyslexia or dyscalculia.
Our data from a patient with early bifrontal brain damage highlight the importance of long-term followup, as the difficulties change from year to year, in keeping with results described by Eslinger et al. [