Article

Arq Neuropsiquiatr 2010;68(6):862-868

Cognitive deficits in patients with mild

to moderate traumatic brain injury
Eliane Correa Miotto1,3, Fernanda Zanetti Cinalli2, Valéria Trunkl Serrao1,
Glaucia Guerra Benute1, Mara Cristina Souza Lucia1,3, Milberto Scaff3

ABSTRACT
Traumatic brain injury (TBI) is one of the most frequent causes of brain damage. Cognitive
deficits reported in the literature after moderate to severe TBI include memory, language,
executive functions, attention and information processing speed impairments. However,
systematic studies on patients with mild TBI are scarce although neuropsychological
changes are present. Objective: To investigate the cognitive functioning of patients with
mild to moderate TBI. Method: We evaluated 12 patients with mild to moderate TBI
using a comprehensive protocol (PN01) of neuropsychological tests. Results: There were
significant deficits of episodic memory including immediate and delayed verbal memory
recall, verbal recognition, immediate and delayed visual memory recall, naming, verbal
fluency and information processing speed. Conclusion: These results emphasize the
importance of comprehensive neuropsychological assessments even in cases of mild TBI in
order to identify impaired and preserved functions providing adequate managing including
rehabilitation programs for each case.
Key words: traumatic brain injury, cognitive deficits, mild to moderate level.

Alterações neuropsicológicas em pacientes com traumatismo crânio encefálico leve-

moderado

RESUMO
Traumatismo craniencefálico (TCE) é uma das causas mais freqüentes de lesão cerebral.
São relatados na literatura déficits cognitivos após TCE moderado-grave relacionados
à memória, linguagem, funções executivas, atenção e velocidade de processamento
de informações. Estudos em pacientes com TCE leve são escassos embora alterações
neuropsicológicas sejam encontradas nestes pacientes. Objetivo: Investigar o
funcionamento cognitivo de pacientes com TCE leve e moderado através de um protocolo
abrangente (PN01) de testes neuropsicológicos. Método: Foram avaliados 12 pacientes
com TCE leve e moderado. Resultados: Foram identificados déficits graves de memória
episódica verbal para evocação imediata, tardia e de reconhecimento, de memória
episódica visuo-espacial para evocação imediata e tardia, nomeação, fluência verbal
nominal e velocidade de processamento de informações. Conclusão: Os resultados do
estudo argumentam a favor da importância de avaliação neuropsicológica abrangente
mesmo em casos de TCE leve a fim de se identificar funções comprometidas e preservadas,
proporcionando condutas e programas de reabilitação adequados a cada caso.
Palavras-chave: traumatismo crânio encefálico, déficits cognitivos, grau leve e moderado.

Correspondence To the World Health Organization in high rates of morbidity and mortality2-4.
Eliane Correa Miotto
(WHO), traumatic brain injury (TBI) is a However, with modern medicine and the
Division of Psychology / ICHC-FMUSP
Av. Dr Enéas de Carvalho 155 public health issue1, because it is one of progress of techniques for acute treatment
05403-900 São Paulo SP - Brasil the largest causes of brain injury, resulting of TBI victims, patient survival rate is in-
E-mail: ecmiotto@usp.br
1
Received 22 July 2009 Division of Psychology, IC, Hospital das Clínicas, University of São Paulo, Medical School, São Paulo SP, Brazil; 2Trainee in
Received in final form 10 June 2010 Neuropsychology, Division of Psychology, IC - Hospital das Clínicas, University of São Paulo, Medical School, São Paulo SP,
Accepted 17 June 2010 Brazil; 3Department of Neurology, University of São Paulo, Medical School, São Paulo SP, Brazil.

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 Cognitive deficits: traumatic brain injury
Arq Neuropsiquiatr 2010;68(6) Miotto et al.

creasing. Consequently, the number of patients who sur- Therefore, this study aimed at investigating the presence
vive with cognitive impairment is growing3-5. of cognitive changes in patients with mild to moderate
TBI severity (mild, moderate, severe) depends on a TBI as well as associations between these changes and
number of factors, including type of injury (diffuse or fo- the localization of brain lesions.
cal), extension and location, resulting in different patterns
of damage2. The Glasgow Coma Scale (GCS) is one of the METHOD
most commonly used tools to evaluate the level of TBI se- Subjects
verity6. It is based on the score for best motor and verbal The subjects were recruited from database that con-
response as well as minimum stimulus to cause eye open- tains all neurological patients treated by the Neuropsy-
ing (Severe Level: 3 to 8; Moderate Level: 9 to 12; and chology staff at Hospital das Clinicas outpatient and ward.
Mild Level: 13 to 15, according to the Advanced Trau- Sixteen patients were evaluated, but 4 were excluded be-
ma Life Support (ATLS), American College of Surgeons cause they did not correspond to the inclusion criteria:
Committee on Trauma, Chicago, 2004). mild to moderate TBI and after 1 year of TBI.
The frontal lobes (especially the orbitofrontal region) The sample included 12 subjects with mild to mod-
and temporal lobes are particularly vulnerable to lesions erate TBI. Patients with less than 1 year of TBI, with co-
caused by TBI2,5,7-9 due to their neuroanatomical local- morbidity or other neurological or healthy problems, in-
ization. Bigler5 emphasizes mesial temporal lobe vulner- cluding use of drugs and alcohol were excluded.
ability, especially the hippocampus, with its connections The Department of Neurology Ethics Committee
to the fornix, associated to persistent post-concussion- FMUSP and CAPPesq (086/06) approved the project and
al syndrome. This syndrome may occur in approximately all participants signed an Informed Consent Term.
15% of mild TBI cases, with changes in attention, memo-
ry, information processing speed and presence of fatigue, Instruments
headaches, nausea, and emotional instability, even when The main instruments consisted of clinical interview
evidence of lesion is not present in brain imaging. Some and neuropsychological tests. The aim of each one is de-
authors argue for functional factors and others for organ- scribed below.
ic factors as the cause of these changes5.
Amongst neuropsychological impairments caused by PN-01 Protocol
mild and moderate TBI, reduction of information pro- Vocabulary (Wechsler Adult Intelligence Scale -
cessing speed7,10-12 is frequently reported in literature and Wais III)20: To investigate verbal abilities and derivation
it may contribute to deficits in attention10,11, orientation of word meaning, which, together with Matrix Reasoning
and executive functioning,7,10-12. Impairments of executive test, provides an estimate Intelligence Quotient (IQ)21;
functions affect mental flexibility, planning, self-monitor- Matrix Reasoning (Wechsler Adult Intelligence
ing, and problem solving2. These impairments can com- Scale - Wais III)20: Non-verbal abilities and non-verbal
promise other abilities, such as attention and memory13,14. logic reasoning, which provide an estimate IQ;
After the period of post-traumatic amnesia (PTA), pa- Hopkins Verbal Learning Test - Revised (HVLT -
tients who experienced severe TBI may present memo- R)22: Episodic memory with immediate, delayed recall
ry disorders of variable intensity15; damages of short term and recognition of verbal information;
and long term7,9-11,16, 17 memory. Brief Visuospatial Memory Test - Revised (BVMT
Changes in behavior and personality may be associ- - R)23: Episodic memory with immediate, delayed recall
ated to TBI, such as reduction in motivation and self-es- and recognition of visual-spatial information;
teem, difficulty with empathy7, emotional processing, loss Digits (Wechsler Adult Intelligence Scale - Wais
of insight, psychosocial difficulties8, post-traumatic stress III)20: Short term memory and working memory;
disorder, depression, anxiety, and fatigue5,7,8,12,18,19. Wisconsin Card Sorting Test (WCST-Nelson ver­
Around two to five years after experiencing mild to sion)24: Mental flexibility, abstraction and problem solving;
moderate TBI, most patients remain stable, even though FAS (COWA – Controlled Oral Word Associa­
some of them present some cognitive difficulties, which tion)25: Nominal verbal fluency, aspect related to execu-
may be observed in daily life tasks7. tive functions, providing evidence of the ability to inhib-
Considering damage variability in cases of TBI2, neu- it irrelevant responses;
ropsychological assessment should be comprehensive al- Category - animals (COWA – Controlled Oral Word
lowing for a systematic analysis of various cognitive func- Association)25: Categorization fluency associated to se-
tions, and providing a background of global functioning mantic memory;
of patients. Studies with systematic neuropsychological Boston Naming Test (BNT)25: Language function:
assessments in patients with mild-moderate TBI are rare. naming;

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Miotto et al. Arq Neuropsiquiatr 2010;68(6)

Symbol Digit Modalities Test26: Information pro- Table 1. Sample distribution according to the area and hemisphere
cessing speed; of the lesion.
Visual Object and Space Perception Battery (Vosp)27: Lesion site N %
Visuoperceptive and visuospatial functions. Parietal R 1 8.33

Temporal R 1 8.33
Procedure
L 1 8.33
All patients were evaluated at the outpatient clinic
of University of São Paulo Neurology Division, Medical Frontal L 4 33.36
School using the PN-01 protocol. The main functions as-
FT R 1 8.33
sessed included memory, language, information process-
L 1 8.33
ing speed, visuospatial, visuoperceptive, executive and in-
tellectual functions. The assessment lasted for two and a FTP R 1 8.33
half hours and was carried out in one day.
TP L 1 8.33
Results were analyzed according to norms of each
standardized test taking into account sample age, gender PO L 1 8.33
and years of education. Descriptive analyses were carried
Total 100
out using SPSS v. 10 (means and standard deviations) of
Right hemisphere - total 4 33.36
percentiles obtained from the norms of each test. This is a
Left hemisphere - total 8 66.64
descriptive study due to the very small sample, that would
not allow for a robust statistical analysis. Total 100
R: right hemisphere; L: left hemisphere; FT: fronto-temporal; FTP; fronto-
temporo-parietal; TP: temporo-parietal; PO: parieto-occipital.
RESULTS
Subjects aged between 25 and 68 years, mean (M)=
39.75 and standard deviation (SD)=14.37, 2 to 13 years of
formal education (M=8.33 and SD=3.39) were evaluated ly on verbal episodic memory (delayed recall and recog-
from November 2006 to May 2008. nition) and presented normal performance on visuospa-
All subjects were evaluated with the GCS (M=12.75 tial episodic memory (recognition), short-term memory,
and SD=2.56), 6 subjects were classified as mild TBI non-verbal skills and Intellectual Quotient (Intellectual
(M=14.8 and SD=0.45) and 6 as moderate TBI (M=11.28 Functions) as described in Table 3.
and SD=2.43). The subjects were evaluated between 12 Patients with right and left hemisphere temporal le-
and 19 months of TBI (M=14.08 and SD=2.02). sions presented moderate to severe deficits in most cog-
Amongst the patients studied, 8 presented left hemi- nitive functions. The results can be seen in Table 4.
sphere and 4 right hemisphere lesions. The majority of Significant impairments were observed on nominal
the patients presented lesions to frontal region (50%), as verbal fluency, naming, and information processing speed
described in Table 1. in patients with left and right frontal-temporal lesions.
The main results showed a significant impairment on The patient with right parietal lesion showed moder-
their information processing speed (M=5.3 and SD=14). ate to severe deficits in most of the functions evaluated,
There were 10 patients showing this deficit accounting with performance within an expected range only on nam-
for 83% of the sample. The second most affected func- ing and non-verbal intellectual abilities.
tion was verbal episodic memory recognition, with 9 The patient with left temporal-parietal lesion present-
(75%) patients presenting significant deficits (M=9.85 ed severe deficits in verbal episodic memory (immedi-
and SD=19.9). Eight (67%) patients presented impair- ate, delayed recall and recognition), naming, categorical
ments in immediate verbal recall (M=10.2 and SD=21.9), verbal fluency, information processing speed and normal
delayed verbal recall (M=9.55 and SD=19.5) and nam- performance on visuospatial immediate and delayed re-
ing (M=18.4 and SD=31.8). Seven (58%) subjects showed call and recognition, short-term memory and visuoper-
an impairment in visuospatial immediate recall (M=20.6 ceptive functions.
and SD=28.5) and nominal verbal fluency (M=8.4 and The patient with right frontal-temporal-parietal lesion
SD=15). Six (50%) patients presented deficits on visuospa- had a moderate to severe impairment on all functions
tial delayed recall (M=28.7 and SD=38.6). Results can be evaluated, except for visuoperceptive functions.
seen in Table 2. The patient with left parietal-occipital lesion showed
In terms of the associations between cognitive chang- a severe difficulty on information processing speed and
es and localization of brain lesions, most patients with left nominal verbal fluency and moderate deficit on intelli-
frontal lesions presented important impairments especial- gence function. His memory, visuoperceptive and visu-

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Arq Neuropsiquiatr 2010;68(6) Miotto et al.

Table 2. Performance average percentiles and standard deviation for right and left hemisphere lesioned patients concerning cognitive
functions and percentile of classified subjects in accordance to standard testing used.
Right hem. Left hem. Classification performance - N (%)
Average of Average of Average of
Cognitive percentile percentile percentile Mild Moderate Severe
Cognitive functions tests (SD) (SD) (SD) Preserved deficit deficit deficit
Verbal episodic memory
Immediate recall HVLT-R 10.2 (21.9) 0.1 (0) 15.3 (25.8) 1 (8) 2 (17) 0 8 (67)
Delayed recall HVLT-R 9.55 (19.5) 3.08 (5.95) 12.8 (23.4) 2 (17) 1 (8) 1 (8) 8 (67)
Recognition HVLT-R 9.85 (19.9) 3.28 (4.55) 13.1 (24) 2 (17) 1 (8) 0 9 (75)

Visualspatial episodic memory

Immediate recall BVMT-R 20.6 (28.5) 3.8 (6.81) 28.9 (31.8) 4 (33) 1 (8) 0 7 (58)
Delayed recall BVMT-R 28.7 (38.6) 3.75 (6.84) 41.2 (42.3) 4 (33) 2 (17) 0 6 (50)
Recognition BVMT-R 15 (10.74) 7.5 (2.88) 18.75 (11.39) 5 (42) 2 (17) 5 (42) 0

Short-term memory
Immediate and Digits 35.5 (35.3) 12.8 (7.5) 46.9 (38.6) 4 (33) 4 (33) 3 (25) 1 (8)
operational

Language
Naming Boston NT 18.4 (31.8) 16.6 (33) 19.3 (33.4) 3 (25) 1 (8) 0 8 (67)

Executive functions
Nom. v. fluency FAS 8.4 (15) 2.8 (3.6) 11 (19) 1 (8) 2 (17) 2 (17) 7 (58)
Categ v. fluency Category 18.7 (24.25) 3.42 (5.72) 26.34 (26.64) 6 (50) 1 (8) 2 (17) 3 (25)
Mental flexibility WCST 32 (29) 33 (36) 26 (28) 5 (42) 1 (8) 2 (17) 4 (33)
IPS Symbol 5.3 (14) 0.1 (0) 7.9 (17) 1 (8) 1 (8) 0 10 (83)
Digit

Intellectual functions
Verbal skills Vocabulary 22 (29) 14 (17) 28 (34) 4 (33) 2 (17) 2 (17) 4 (33)
Non-verbal skills Matrix 38 (37) 28 (36) 43 (39) 6 (50) 1 (8) 3 (25) 2 (17)
reasoning
IQ 24 (29) 11 (17) 30 (33) 5 (42) 0 5 (42) 2 (17)

Visuo-perceptive functions
Incomplete VOSP 44.8 (34.1) 25.8 (35.8) 54.3 (31.1) 10 (83) 0 0 2 (17)
Letters
Position VOSP 44 (26.8) 23.6 (26.1) 54.3 (21.9) 8 (67) 2 (17) 1 (8) 1 (8)
Discrimination
SD: standard deviation; Hem.: hemisphere; N: number; IPS: information processing speed; IQ: intellectual quotient; HVLT-R: Hopkins Verbal Learning Test -
Revised; BVMT-R: Brief Visualspatial Memory Test - Revised; Boston NT: Boston Naming Test; Nom. V. fluency: Nominal verbal fluency; Categ. V. fluency: category
verbal fluency; WCST: Wisconsin Card Sorting Test; VOSP: Visual Object and Space Perception Battery.

ospatial functions, mental flexibility and categorical ver- Episodic memory and executive processes related to
bal fluency were preserved. encoding, storage and retrieval, together with strategy
formulation, were the main altered cognitive functions.
DISCUSSION In the literature, these changes are observed especially in
This study aimed at evaluating overall cognitive per- moderate to severe cases of TBI13.
formance of patients diagnosed with mild to moderate Most patients presented some level of difficulty, from
TBI, by means of The PN-01, a systematic protocol. The mild to severe, on the administered tests. Nevertheless,
main results showed significant deficits in information in two of the 16 functions evaluated, they showed normal
processing speed, memory (verbal and visuospatial), lan- performance including on visuoperceptive and visuospa-
guage (naming) and executive functions. tial functions. This finding can be possibly explained by

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Miotto et al. Arq Neuropsiquiatr 2010;68(6)

Table 3. Average percentile and standard deviation and classification performance of patients with left frontal lesions concerning cognitive
functions.
Frontal left lesions

Average of Classification performance - N (%)

Cognitive function percentile (SD) Preserved Mild deficit Moderate deficit Severe deficit
Verbal episodic memory
Immediate recall 23.3 (35.9) 1 (25) 0 2 (50) 2 (50)
Delayed recall 6.9 (13.4) 1 (25) 0 0 3 (75)
Recognition 0.22 (0.25) 0 0 0 4 (100)

Visualspatial episodic memory

Immediate recall 27.9 (33.6) 2 (50) 0 0 2 (50)
Delayed recall 34.8 (40.1) 2 (50) 0 0 2 (50)
Recognition 21.5 (11) 3 (75) 0 1 (25) 0

Short-term memory
Immediate and operational 71.2 (38.3) 3 (75) 1 (25) 0 0

Language
Naming 26.1 (43.1) 1 (25) 1 (25) 0 2 (50)

Executive functions
Nominal verbal fluency 21.5 (22.6) 1 (25) 1 (25) 0 2 (50)
Category verbal fluency 14.8 (7.1) 2 (50) 1 (25) 0 1 (25)
Mental flexibility 28.8 (24.6) 2 (50) 1 (25) 0 1 (25)
IPS 15.1 (23.8) 1 (25) 1 (25) 0 2 (50)

Intellectual functions
Verbal skills 43.7 (41.98) 2 (50) 1 (25) 0 1 (25)
Non-verbal skills 57.7 (40.1) 3 (75) 0 1 (25) 0
IQ 46.2 (39.3) 3 (75) 0 1 (25) 0

Visuoperceptive functions
Incomplete letters 63.8 (24.5) 4 (100) 0 0 0
Position discrimination 46.5 (30.9) 3 (75) 0 0 1 (25)
SD: standard deviation; IPS: information processing speed; IQ: intellectual quotient.

the preservation of occipital and posterior brain areas in ing speed in patients with left and right frontal-tempo-
many of the patients. ral and left parietal-occipital lesions. These findings are
Most patients had frontal and temporal lesions and in line with the literature showing participation of frontal
these regions are known to be particularly vulnerable and temporal areas in processes such as encoding, stor-
to cognitive deficits related to memory and executive age, and retrieval of information, in addition to, strategy
functions2,5-8,14. Patients with left frontal lesions present- and information processing speed13.
ed more difficulties on verbal episodic memory, on both One limitation of the study is the relatively small num-
recognition and delayed recall, as well as, on executive ber of samples, which did not allow for a robust statisti-
functions. cal analysis. In spite of the small sample, it was possible to
Patients with right and left hemisphere temporal le- demonstrate that even mild to moderate TBI patients may
sions presented a moderate to severe difficulty in most show a range of mild to severe deficits in a variety of cog-
cognitive functions as patients with right parietal, left tem- nitive functions. It is possible that, since PN01 is a detailed
poral-parietal and right frontal-temporal-parietal lesions. and systematic protocol, the current study was able to show
In addition, cognitive impairments were observed on a wide range of cognitive impairments in these subjects.
nominal verbal fluency, naming and information process- The current results also suggest that a systematic neu-

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Arq Neuropsiquiatr 2010;68(6) Miotto et al.

Table 4. Classification performance of patients concerning localization of brain lesions and cognitive functions.
Classification performance concerning lesion localization (Percentile)
Parietal Temporal Frontal temporal FTP TP PO
Cognitive function Right Right Left Right Left Right Left Left
Verbal episodic memory
Immediate recall Sev. (<1) Sev. (<1) Sev. (1) Sev. (<1) Mod. (8) Sev. (1) Sev. (<1) Mild (21)
Delayed recall Sev. (<1) Sev. (<1) Sev. (1) Mild (12) Mod. (8) Sev. (1) Sev. (<1) Pres. (66)
Recognition Sev. (1) Sev. (2) Sev. (1) Mild (10) Pres. (50) Sev. (<1) Sev. (<1) Pres. (54)

Visualspatial episodic memory

Immediate recall Sev. (1) Sev. (<1) Sev. (1) Mild (14) Sev. (<1) Sev. (<1) Pres. (50) Pres. (69)
Delayed recall Sev. (<1) Sev. (<1) Sev. (1) Mild (14) Mild (10) Sev. (<1) Pres. (96) Pres. (84)
Recognition Mild (10) Mod. (5) Mod. (5) Mild (10) Mod. (5) Mod. (5) Pres. (27) Pres. (27)

Short-term memory
Immediate and operational Mod. (9) Mild (24) Sev. (<1) Mild (9) Mild (24) Mod. (9) Pres. (50) Mild (16)

Language
Naming Pres. (66) Sev. (<1) Sev. (<1) Sev. (<1) Sev. (<1) Sev. (<1) Sev. (<1) Pres. (50)

Executive functions
Nominal verbal fluency Sev. (2) Mod. (8) Sev. (<1) Sev. (1) Sev. (<1) Sev. (<1) Mod. (3) Sev. (<1)
Category verbal fluency Mild (12) Sev. (<1) Mod. (7) Sev. (<1) Mild (24) Sev. (<1) Sev. (<1) Pres. (46)
Mental flexibility Sev. (<1) Pres. (50) Sev. (<1) Pres. (75) Mod. (9) Sev. (2) Mod. (9) Pres. (75)
IPS Sev. (<1) Sev. (<1) Sev. (<1) Sev. (<1) Sev. (<1) Sev. (<1) Sev. (2) Sev. (<1)

Intellectual functions
Verbal skills Sev. (2) Mild (14) Sev. (<1) Pres. (37) Mod. (9) Sev. (1) Pres. (34) Mod. (4)
Non-verbal skills Pres. (37) Sev. (<1) Mod. (5) Pres. (75) Pres. (84) Sev. (1) Mod. (5) Mild (21)
IQ Mod. (5) Mod. (3) Sev. (2) Pres. (37) Pres. (37) Sev. (<1) Mod. (9) Mod. (9)

Visuoperceptive functions
Incomplete letters Sev. (<1) Sev. (<1) Sev. (<1) Pres. (27) Pres. (76) Pres. (76) Pres. (76) Pres. (27)
Position discrimination Mild (14) Mod. (4) Pres. (62) Pres. (62) Pres. (62) Mild (14) Pres. (62) Pres. (62)
FTP: frontal temporal parietal lesion; TP: temporal parietal lesion; PO: parietal occipital lesion; IPS: information processing speed; IQ: intellectual quotient; Sev.:
severe; Mod.: moderate; Pres.: preserved.

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