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Vol. 27. Num. 3.May - June 2016Pages 103-154
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Vol. 27. Num. 3.May - June 2016Pages 103-154
Case Report
DOI: 10.1016/j.neucir.2015.09.001
Adolescents with vascular frontal lesion: A neuropsychological follow up case study
Adolescentes con lesión vascular frontal: seguimiento neuropsicológico de estudio de casos
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Clara L. Cháveza,b,c,
Corresponding author
clara.chavezarana@mcri.edu.au

Corresponding author.
, Guillermina Yáñeza, Cathy Catroppab,c, Sulema Rojasa, Erick Escartina, Stephen J.C. Hearpsb, Antonio Garcíad
a Universidad Nacional Autónoma de México, FES Iztacala, México, D.F., Mexico
b Child Neuropsychology, Murdoch Children's Research Institute, Melbourne, Victoria, Australia
c University of Melbourne, Victoria, Australia
d Medical Unit of High Specialty “La Raza” IMSS, Paediatric Neurosurgery Service, México, D.F., Mexico
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Tables (3)
Table 1. Demographic characteristics of the participants.
Table 2. Significant clinical changes in cognitive functions, standard scores, and reliable changes index.
Table 3. Significant clinical changes in executive function, standard scores and reliable change indexes.
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Abstract

The objective of this research was to identify clinically significant changes in cognitive functions in three adolescents who underwent surgery for resection of a focal vascular lesion in the frontal lobe. Cognitive functions, executive function, behavior regulation, emotion regulation, and social abilities were assessed prior to surgery, six and 24 months post-discharge. Significant clinical changes were observed during all the assessments. Cognitive changes after surgery are not homogeneous. Most of the significant clinical changes were improvements. Especially the significant clinical changes presented in EF domains were only improvements; these results suggest that EF were affected by the vascular lesion and benefitted by the surgery. After resection of a vascular lesion between 15 and 16 years of age the affected executive functions can continue the maturation process. Our results highlight the importance that assessments must include emotional aspects, even if deficits in these domains are not presented in the acute phase. Rehabilitation methods should promote the development of skills that help patients and their families to manage the emotional and behavioral changes that emerge once they are discharged from the hospital.

Keywords:
Adolescents
Executive functions
Brain lesions
Neurosurgery
Arteriovenous malformations
Cavernous angioma
Resumen

El objetivo de este estudio fue identificar cambios clínicamente significativos en las funciones cognoscitivas de tres adolescentes que fueron intervenidos quirúrgicamente para resección de una lesión vascular focal en el lóbulo frontal. Se midieron funciones cognoscitivas, funciones ejecutivas, regulación conductual, regulación emocional y habilidades sociales en tres momentos, antes de la cirugía, 6 y 24 meses después de la cirugía. Se observaron cambios clínicamente significativos durante los tres momentos de evaluación. Los cambios cognoscitivos después de la cirugía no son homogéneos. La mayoría de los cambios fueron incrementos. Especialmente los cambios clínicamente significativos presentados en funciones ejecutivas fueron mejoras, los resultados sugieren que la resección de una lesión vascular entre los 15 y 16 años de edad permite la recuperación de las funciones ejecutivas. Nuestros resultados señalan la importancia de incluir aspectos emocionales en la evaluación, aún si no se presentaron alteraciones emocionales en la fase aguda. Se sugiere que los métodos de rehabilitación apoyen a los pacientes y a sus familias a manejar los cambios emocionales y conductuales que surgen una vez que son dados de alta del hospital.

Palabras clave:
Adolescentes
Funciones ejecutivas
Lesiones cerebrales
Neurocirugía
Malformaciones arteriovenosas
Hemangioma cavernoso
Full Text
Introduction

The cognitive processes involved in the conscious control of thought and action are called executive functions (EF).1 EF is a psychological construct composed of multiple interrelated cognitive functions such as anticipation and deployment of attention, impulse control, self-regulation, initiation of activity, working memory, mental flexibility, utilization of feedback, planning, organization and selection of problem solving strategies.2 EF are essential to learn new skills, apply knowledge to real life situations, establish our autonomy from the environment and provide capacity for reflection.3,4 These cognitive functions are largely mediated by the prefrontal cortex (PFC).5 Research has tried to explain the relation between changes in the PFC and changes in EF observed during adolescence.6–10 Some studies suggest that cognitive development observed during adolescence is related to gray matter pruning, while others observed that the increase of white matter provides better connectivity between cortical and subcortical regions, which underlie executive functions.8–11

Developmental studies show that during adolescence brain maturation is linked to efficiency on executive tasks. Cognitive flexibility matures between the 7 and the 10 years, earlier than planning and working memory.2,12 At 12 years of age there is an improvement in goal directed behavior, between 14 and 17 years of age, adolescents improve their decision making, including affection, at 15 years of age there is an improvement in attention control and speed processing and between 16 and 19 years of age there are gains in working memory, planning and solution problems.2 Cognitive functions are interrelated, speed of processing, inhibition and working memory develop in an independent way, but speed of processing and inhibition have a direct influence on the development of working memory.13 EF have an important role in social abilities.14 Social interactions require cognitive functions such as judgment, self-regulation, and organization of new information; problem solution and theory of mind.14 The development of intact social skills depends on the maturation of brain, cognition (attention, executive skills, communication and social cognition) and behavior, within a supportive environmental context.15

The PFC myelination begins before birth and is completed during the third decade of life.16 An acquired brain injury in the prefrontal cortex during adolescence may disrupt the maturation process of executive functions.16–18 Brain injuries that can be detected during adolescence include vascular lesions, such as arteriovenous malformations (AVM) and cerebral cavernous angioma. AVM in children is a rare neurologic insult that occurs in less than 1% of children, “an AVM is an abnormal collection of blood vessels in which arterial blood flows directly into the draining vein without the normal interposed capillaries” (p.01).19 The AVM draw blood away from normal vessels and the volume of blood directed to the AVM increases, as a consequence ischemia of the regions around the vascular lesion is presented, this is call the “blood steal phenomenon”. The treatment for AVM is the complete resection of the vascular lesion to prevent future hemorrhage and to preserve and restore neurologic function, while its success will depend on the location, size and hemodynamic properties of the AVM together with the clinical condition of the patient.19 On the other hand, cavernous angiomas of the brain are rare.20 The prevalence of cavernous angioma is of 0.4–0.5% in the general population, 8–15% of these cavernous are located in the brain and spinal cord.21 A cavernous angioma is composed of irregular sinusoidal vascular structures without intervening nervous parenchyma, and there may be tiny vessels afferent, efferent and draining veins. Patients with cavernous angioma can be treated by administration of anticonvulsants or surgically, however, surgical intervention may have more benefits than medical interventions, in fact early surgical intervention provides more effective results.22

Study cases of cognitive outcomes of vascular lesions during childhood or adolescence report a strong relationship between the cognitive outcomes and the localization of the lesion and adjacent areas.23–25 Whingham and Otoole Biddle25 reported that regardless of the AVM location, participants presented with mild to moderate deficits in EF. Which has also been observed in children and adolescents with acquired brain injury who usually present deficits in EF.26,27

Age of onset is a factor to take in consideration for the cognitive outcomes of brain injuries, because some deficits emerge years later, when the social demands increase.17 Longitudinal study cases of AVM in children showed that the cognitive outcomes change over time, while some cognitive functions improve, cognitive functions related to the localization of the lesion tend to deteriorate over time.28,24

There is very little information about cognitive outcomes of vascular lesions during adolescence.17 One reason may be that in 95% of the cases the symptoms are evident between the second and the third decade of life.19 Despite the fact that the cognitive consequences of a brain insult during a development period will become evident over time,17 longitudinal studies in this area are rare, with only case studies found, but it is unclear how significant changes over time were identified.25 The objective of this research is to study the neuropsychological outcomes of three adolescents who underwent surgery for resection of a vascular focal frontal lesion (AVM and cavernous angioma) and who were followed up for two years post-surgery. This information is necessary to give an accurate prognosis together with an appropriate intervention.

MethodsParticipants

During the recruitment period six adolescents were admitted to the Pediatric Neurosurgery Service of the Medical Unit of High Specialty “La Raza” IMSS, México, with a diagnosis of a vascular frontal lesion. One of the patients was ineligible for the study because she did not need surgery. The assessments before surgery and at 6 months after discharge were possible with five participants.

Two participants were unable to be located for the final assessment. Three adolescents (50% of the original simple) participated in the 2-year follow-up; these adolescents had a diagnosis of vascular frontal lesion and had been originally recruited from Pediatric Neurosurgery Service of Medical Unit High Specialty “La Raza”, México; between September 2009 and April 2010. Inclusion criteria were: (i) age between 15 and 16 years at surgery, (ii) medical records that determine a vascular lesion in the frontal lobe, and (iii) surgery for resection of the vascular lesion. Exclusion criteria were: (i) more than one brain surgery (ii), rehabilitation after surgery, and (iii) evidence of pre-existing physical, neurological, psychiatric, or developmental disorder.

Table 1 shows demographic information of the three adolescents that participated in the 2-year follow-up.

Table 1.

Demographic characteristics of the participants.

Case  Case 1  Case 2  Case 3 
Sex  Male  Male  Male 
Injury age (years, months)  15, 2  16, 3  15, 1 
Injury type  Cavernous angioma  AVM  AVM-IV 
Region of injury  Right frontal lobe  Right frontal lobe  Left frontal lobe 
Surgical intervention  Yes  Yes  Yes 
Neurological signs before surgery  Yes  Yes  No 
Case 1

Case 1 is a 15-year-old male at time of recruitment, he had a cavernous angioma in the right frontal lobe, which was detected after he presented with a seizure. He had measles at 7 years of age, since 7 years of age he has been wearing glasses, he is allergic to dust and dog hair, but had not needed drug treatment. He had good eating, sleeping and hygiene habits. His family had no history of cavernous angioma. His mother's pregnancy lasted 7 months, he was born by emergency cesarean section because of neonatal hypoxia, and so he was in an incubator for a few days. According to parents, he presented with normal motor and language development. He always had good school performance, and at time of recruitment he was in third year of high school, after surgery he continued studying. During the assessment he was cooperative, however presented with introverted behavior. His mother was very supportive at the time of the injury and continued this role during the three assessments. The family members shared a good relationship. Before surgery he was medicated with levetiracetam, and after surgery he was medicated with phenytoin (PHT) for a month.

Case 2

Case 2 is a 16-year-old male with a cerebral AVM on the right frontal lobe, before surgery he presented with three seizures. His AVM according to Spetzler grading system was grade 1, because it was 3cm in size. His mother's pregnancy lasted 9 months without complications. He had good eating, sleeping and hygiene habits. He presented with normal motor and language skills, and good school performance. At the time of the recruitment he was completing the last year of high school and by the last follow-up assessment he had finished high school and started to work at a tyre shop. His family was very interested in the assessment results and accompanied him to every feedback. Before surgery he was treated with phenytoin, after surgery he continued his treatment with PHT for 12 months.

Case 3

As can be seen in Table 1, Case 3 was a 15-year-old male when the AVM was detected on his left frontal lobe, after, he presented with loss of consciousness, vomiting and right hemiparesis, and 3 months previous he had presented with persisting headaches. His mother's pregnancy lasted 9 months without complications and his motor and cognitive development had been normal. According to Spetzler grading system his AVM was grade IV. After surgery he was treated with ranitidine, dexamethasone and PHT for a few days. He appeared to be well supported by his mother. In the last assessment he had finished high school, but he did not have future plans.

Measures

Cognitive functions, EF, behavior regulation, emotional regulation and social skills were assessed with the same instruments in the three assessment phases.

Cognitive functions

The Wechsler Intelligence Scale for Children-IV [WISC-IV29] or the Wechsler Adult Intelligence Scale [WAIS-III30] was administered, depending on the age of participant (WISC-IV<16.11 years, WAIS-III>16.0 years). Verbal Comprehension Index (VCI: M/100, SD/15), Perceptual Reasoning Index (PRI: M/100, SD/15) and Full Scale IQ (FSIQ: M/100, SD/15) were used in analyses. VCI is a measure of general verbal skills, while PRI is an index obtained through non-verbal tasks, measures visual-spatial organization and visual-motor skills.

Executive functions

  • (i)

    Cognitive flexibility. Standard scores (M/50, SD/10) for the perseverative answers (M/50, SD/10) from the Wisconsin Card Sorting Test [WCST31] were used to study cognitive flexibility. This task requires the participant to shift cognitive strategies in response to environmental changes.

  • (ii)

    Response inhibition. Resistance interference index (M/50, SD/10) from the Stroop Color and Word Test [Stroop32] measures response inhibition. The test is based on the observation that individuals can read words much faster than they can identify and name colors, the task requires the participant to inhibit reading and name of the color in which words are written, this condition places the highest demands on response inhibition. Resistance interference index (M/50, SD/10) was used to measure inhibition.

  • (iii)

    Planning and rule following. The Towel of London Test [TOL33], was used to measure planning and rule following. Standard scores (M/100, SD/15) for the total Achievement Score, based on the total number of moves and rule violation, were used in the analyses.

  • (iv)

    Working memory. Working memory index from WISC-IV29 and WAIS-III30 are indexes obtained from various tasks that assess the ability to memorize new information, hold it in short-term memory, concentrate and manipulate that information to produce some result. These indexes were used to measure working memory (WMI: M/100, S/15).

  • (v)

    Processing speed. Processing Speed Index from WISC-IV29 and WAIS-III30 is an index obtained from several subscales that measures the speed at which cognitive processes can be carried out. This index was used to measure processing speed (SPI: M/100, SD/15).

Emotional regulation, behavior regulation and social abilities

The Parent Rate Scales of the Behavior Assessment System for Children and Adolescents [BASC34] was employed, which included 123 items for which parents responded according to the frequency of the behavior observed. We used four domains derived from the clinical scale, aggression and hyperactivity domain's were used to measure behavior regulation; depression and anxiety domain's were used to measure emotion regulation. These domains have a mean of 50 and standard deviation of 10 points, with a higher score indicating greater behavioral disturbance, and scores of 70 or more considered to represent behavioral difficulties of clinical significance. Social skills and leadership are derived from the adaptive scale; we used these domains to measure social abilities. These domains have a mean of 50 and standard deviation of 10 points, but higher scores indicate better social skills.

Procedure

Adolescents were enrolled in the study during their initial hospital admission. The participants and at least one of their parents were given a detailed description of the study and asked to provide written consent as per ethics requirements. Once they had agreed to participate, parents were requested to give a contact phone number to make the future appointments for the assessments. Three assessments took place: before surgery (T1), 6 months after being discharged (T2) and 2 years after being discharged (T3). A neuropsychologist at the hospital assessed adolescents individually and the tests were administered in fixed order, after each assessment they received a report with their results.

Analysis

When neuropsychological tests are re-administered, test scores may fluctuate, because the tests are not perfectly reliable and many people fluctuate in their functioning from time to time.35 Therefore, in this study we decided to use the Reliable Change Index (RCI) that identifies when change in an individual's score is clinically significant and reflect the fluctuation of an imprecise measuring instrument.36 The RCI is equal to the pre-test score minus their post-test score divided by the standard error of the difference of the test. A RCI of 1.96 or greater reflects a significant clinical change (p<.05). In this study the RCI was obtained comparing the results of T1–T2 and T1–T3.

Results

Results for VCI, PRI and Full Sale IQ were calculated and are presented in Table 2.

Table 2.

Significant clinical changes in cognitive functions, standard scores, and reliable changes index.

  Case  Standard scoreRCI
    T1  T2  T3  T1–T2  T1–T3 
VCI  Case 1  100  110  86  a+2.90  a−4.06 
  Case 2  79  95  82  a+4.64  +.87 
  Case 3  69  95  84  a7.54  a+4.35 
PRI  Case 1  82  90  78  a+2.11  −1.058 
  Case 2  94  90  109  −1.05  a+3.96 
  Case 3  90  96  99  +1.58  a+2.38 
Full Scale IQ  Case 3  72  92  81  a+4.72  a+2.12 

T1, before surgery assessment; T2, six months after being discharged assessment; T3, 2 years after being discharged assessment; RCI, reliable change index; VCI, verbal comprehension index, PRI, perceptual reasoning.

a

Significant change.

The three cases presented significant clinical changes in verbal comprehension and perceptual reasoning, while only Case 3 presented clinical significant change in Full Scale IQ.

Table 3 shows results calculated for executive functions, behavior regulation, emotional regulation and social abilities.

Table 3.

Significant clinical changes in executive function, standard scores and reliable change indexes.

  Case  Standard scoreRCI
    T1  T2  T3  T1–T2  T1–T3 
Perseverative answersCase 1  35  33  51  −0.22  1.76 
Case 2  35  27  67  −0.88  a+3.52 
Case 3  37  35  55  −0.22  a+1.98 
Rule violationCase 1  72  60  104  −.98  a+2.01 
Case 2  78  104  104  a+2.12  a+2.01 
Inhibition response  Case 3  16.2  40.64  46  a+2.105  a+2.56 
WMI  Case 1  83  91  100  +1.19  a+2.54 
PSI  Case 3  62  88  98  a+4.58  a+6.34 
Aggression  Case 3  38  41  55  0.354  a+2.006 
Hyperactivity  Case 1  47  33  31  a−1.994  a−2.279 
Depression  Case 3  55  52  82  −0.486  a+4.374 
Anxiety  Case 2  62  68  50  .804  −1.609 
Social skillsCase 2  35  48  50  a+2.01  a+2.23 
Case 3  53  54  33  0.15  a−3.10 
LeadershipCase 1  52  71  53  +2.95  +0.15 
Case 2  46  52  64  0.93  a+2.79 

T1, before surgery assessment; T2, six months after being discharged assessment; T3, 2 years after being discharged assessment; RCI, reliable change index; WMI, working memory index, PSI, processing speed index.

a

Significant change.

As Table 3 shows, Case 1 presented with significant clinical improvement in rule following and working memory overtime, Case 2 presented with significant clinical improvement in cognitive flexibility, and rule following, while Case 3 presented with significant clinical improvement in cognitive flexibility, inhibition response and speed processing. As can be seen in Table 3, Case 1 presented a significant clinical improvement in social skills and behavior regulation, Case 2 presented with significant clinical improvement in emotional regulation and social skills, while Case 3 presented significant clinical deterioration in behavior regulation, emotional regulation and social skills over time.

DiscussionCognitive functions

Cognitive function domains included verbal comprehension, perceptual reasoning and IQ. Case 1 who had a cavernous angioma on the right frontal lobe showed an improvement followed by a decrease in verbal comprehension and perceptual reasoning, the results obtained in the last assessment where lower than those obtained in the pre-surgery assessment. Case 2 who had an AVM in the right frontal lobe showed an improvement in verbal comprehension between T1 and T3. During the first six months after surgery he did not show clinical significant changes in perceptual reasoning, later he showed improvement between T2 and T3. Case 3 who had an AVM in the left frontal lobe progressively improved in verbal comprehension and perceptual reasoning. These results suggests that when a brain insult occurs during adolescence significant clinical changes can be observed 2 years after surgery, the results are consistent with previous literature17 that mentioned that the consequences of a brain insult during development period became evident over time. The results highlight the importance of longitudinal studies and the assessment at different time periods after surgery. Case 3 was the only participant that presented with changes in IQ; he improved 10 points between T1 and T3. The results show that in cerebral vascular lesions IQ is not a sensitive measure of cognitive changes, so it is important to assess specific cognitive functions related to the affected brain region.

Executive functions

Regard to identify significant clinical changes in executive functions of adolescents with vascular frontal lesions. According to literature, planning shows a significant increase in this function during adolescence, in comparison with pubescence, teenagers are faster at solving planning tasks.2,37 In the cases studied in this work the injury did not disrupt the maturation of this function, since at the three times of assessment adolescents had similar performance to the normative group of the tests and they did not present significant with clinical changes between the assessments.

The results showed that executive function deficits identified before surgery improved over time.17 In the assessment before surgery Case 2 had difficulties on tasks of mental flexibility and rule following, but over time reached the expected level of development for his age. Case 3 presented with deficits in mental flexibility, response inhibition and speed processing on assessment before surgery, but in the last assessment he no longer had these deficits. The same pattern was observed for Case 1, he initially had deficits in metal flexibility and a working memory with scores corresponding to a low average range, but over time both functions improved. All the significant clinical changes presented in EF where improvements, therefore this suggest that executive functions can recover after the resection of a brain vascular lesion in the frontal lobe during adolescence. This can be a consequence of surgery, one hypothesis is that after surgery the regions affected by the steal phenomenon are better irrigated and as a consequence the cognitive functions that were affected by the vascular lesion improve and continue de maturation process.

It has been reported that cognitive flexibility matures between 7 and 10 years,12 in this study, in T1 and T2 assessments the participants obtained scores two standard deviations below the mean. However, in the last assessment they presented with a significant clinical improvement, suggesting that mental flexibility is sensitive to vascular lesions when it presents during adolescence, however it can recover and continue the maturation process after 15 years of age. Another hypothesis is that after surgery, the brain can work better as a whole and therefore EF improved.

Before surgery Case 1 presented with one seizure and Case 2 presented with three seizures. EF deficits showed in the first assessment could be related to the seizures, although EF deficits are related with high frequency of seizures,38 which was not a characteristic of the participants in this study. The three cases were treated with phenytoin after surgery, Case 1 for a month, Case 2 for 12 months and Case 3 for a few days. PHT had been related to deficits in attention, speed processing and working memory.39 The cognitive deficits showed by Case 2 during the second assessment could be related to the PHT treatment. On the other hand, people who underwent craniotomies are in high risk of presenting subsequent seizures.40 PHT had shown to be effective in reducing the risk of presenting subsequent seizures after neurosurgery.40 The participants in this study were treated with PHT and did not present subsequent seizures. This may suggest that the improvements showed in EF are a result of the resection of the vascular lesion in combination with the anticonvulsant treatment as a preventer of subsequent seizures.

Behavior and emotional regulation

The literature reports that the control systems of the prefrontal cortex continue the maturation during adolescence.8 It is also reported that the frontostriatal circuit continues to develop during adolescence.41 In the last assessment Case 3 presented aggressive behavior and this can be a consequence of an alteration in the development of the prefrontal cortex, in the other hand the hyperactive behavior of Case 1 decrease, in this case the maturation process of the prefrontal cortex was slightly affected in the presence of the lesion, however, the maturation process retook its course. In this regard Case 3 in the last assessment showed features of depression, while the anxiety of Case 2 decreased. The outcomes in behavior and emotional regulation could also be affected by environmental factors,42 however in this study those factors were not measured.

Social abilities

In this regard the social abilities of Case 3 decrease in the last assessment. Although his EF (mental flexibility, responses inhibition and speed processing), verbal comprehension, perceptual reasoning and IQ improved, his social abilities decreased, this may be due to the features of depression, since it has been mentioned15 that adequate social skills depend on cognitive, emotional and linguistic functions and internal and external mediators.

Case 2 in the first assessment show deficits in mental flexibility, rule following and social abilities, in the last assessment this executive functions and his social abilities improved, this may be due to the interaction of the executive functions with the social interactions reported in literature.2,14,15 Most of the significant clinical changes in behavior regulation, emotional regulation and social abilities where identified in the last assessment, these results demonstrate the importance of monitoring adolescence with frontal lesions over time and include emotional domains in the assessment. These results highlight the importance rehabilitation methods that help patients to develop behavior regulation, emotion regulation and social skills.

Our findings are consistent with previous studies where in the three cases we found a relationship between the neuropsychological outcomes and the localization of the AVM.23 Case 3 who had an AVM in the left frontal lobe presented with verbal comprehension deficits, and prior to surgery the three participants presented with deficits in different domains of executive function. Sumiyoshi et al.,43 described a case of a preadolescent with a cavernous angioma in which the neuropsychological deficits were related to the localization of the lesion, for Case 1 we found similar neuropsychological outcomes, the difficulties he presented matched with the region of the lesion.

Limitations and future directions

The interpretation of results from this study is somewhat limited due to the small sample size, future longitudinal studies may include a larger sample size to make generalizations about specific neuropsychological profiles expected in these patients. Another limitation is that in the last assessment, participants were between 17 and 18 years old, so the development of their prefrontal cortex was continuing, therefore another assessment as adults could provide a clearer idea of the definite outcomes of the vascular lesion. All the participants underwent surgery, so we cannot be sure if the changes observed were because of the surgery, so longitudinal studies in vascular lesions with and without undergoing surgery will provide us with further information, however this may be difficult to design because such lesions are generally treated with surgery.

Conclusion

Cognitive changes after surgery are not homogeneous. EF and some cognitive functions seem to improve significantly, while other cognitive functions deteriorate over time. We should highlight that most of the significant clinical changes observed in the studied variables after surgery were improvements. Especially the significant clinical changes presented in EF domains were only improvements; these results suggest that EF's that were affected by the vascular lesion benefitted by the surgery. The results indicate that after the resection of a vascular lesion in the frontal lobe between 15 and 16 years old, EF's that were affected by the lesion can continue de maturation process. The results highlight the importance that assessments must include emotional aspects, even if deficits in these domains are not presented after surgery. Rehabilitation methods should promote the development of skills that help patients and their families to manage the emotional and behavioral changes that emerge once they are discharged from the hospital.

Conflict of interest

The authors declare no conflict of interest.

The participants and their parents were informed and signed consent.

Funding

The study received support from The National Council for Science and Technology CONACYT.

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