Study of EEG Changes Among Sample Of Egyptian Children With Attention Deficit Hyperactivity Disorder

Document Type : Original Article

Authors

1 Neuropsychiatry department,Police Academy Hospital,Egypt

2 Psychiatry department, Al Al-Azhar University, Cairo, Egypt.

3 department of psychiatry, faculty of medicine, Al-Azhar university, Cairo, Egypt

4 Lecturer of psychiatry Al-Azhar university

Abstract

Background: Attention Deficit Hyperactivity Disorder(ADHD) is a mental Neuro-developmental type, Up to 5% of primary school-age children have ADHD, characterized by Inattention, Hyperactivity ,and Impulsivity, Relation between Encephalography (EEG) and (ADHD) is ambiguous, Guidelines recommend that (EEG) indicated only in the clinical suggestions of seizure disorder or a presence of focal signs.
Aim: To Study the Relation Between (ADHD) children and Their (EEG) changes, Further study of the Efficacy of Atomoxetine\Antipsychotic and Antiepileptic on ADHD children.
Subjects and Methods: 60 Egyptian children (age 6-18) with No previous history of seizures. They had been attending to Neuropsychiatry clinic for treatment and fulfilling the criteria for (ADHD) according to (DSM-IV), Conner's scale for (ADHD) and (EEG) was applied for 60 children. Follow up study was conducted from September 2018 to January 2021, included, Follow up of all children with their treatment of all types of (ADHD) using Atomoxetine, Atomoxetine/Antipsychotic combination ,and Antiepileptic.
Results: Out of 60(ADHD) children, only 6 children showed (EEG) Abnormalities, Atomoxetine showed superior efficacy on(ADHD) inattention type , Atomoxetine/Antipsychotic Combination Showed Superior efficacy on(ADHD)Hyperactivity type and(ADHD)Combined type. while Antiepileptic Showed a frustrating improvement on NON- epileptic(ADHD)regardless the type of it.
Conclusion: There is NO correlation observed between NON-epileptic (ADHD) children and their EEG abnormalities, In addition, there were NO improvement noticed for Antiepileptic on NON- epileptic(ADHD)children.

Keywords


INTRODUCTION

Attention deficit hyperactivity disorder is a common developmental condition of inattention that might be accompanied by hyperactivity or not .1

ADHD is characterized by difficulty paying attention, excessive activity ,and behavior regardless of the consequences which are not appropriate for a person's age.2

Diagnosis of ADHD using EEG is an ongoing area of investigation in the united states, the food and drug administration has approved the use of EEG to only evaluate the morbidity of ADHD . 3

A wide agreement that ADHD occurs as a result of dysfunction in the central nervous system, but the mechanism are still not well known, EEG is used to describe as well as to quantify the neurophysiology of ADHD, also clinically the assessment, diagnosis ,and treatment of ADHD. 4

The EEG common features related with ADHD is the elevation of slow waves Theta and/or decreased power of  fast waves Beta, mostly noticed on the fronto-central electrodes, which are sometimes combined and quantified by the theta/beta ratio TBR . 5

Not less than five recent studies failed to duplicate theta/beta ratio TBR differences in ADHD versus Non-ADHD between groups of children and adults, as well as cross-sectional across age. 6

In a study of 101 children, only 62 were diagnosed with ADHD differentiating between children with and without ADHD based on theta/beta ratio TBR reported an accuracy of 89.9-96.5% in theta/beta ratio predicting age but only 49.2-54.8% accuracy in predicting if the individual has ADHD or not. 7

Another study suggests the EEG theta/beta ratio is not definitive in differentiation between individuals with or without ADHD. 8

The slight success of  EEG in the diagnosis of ADHD is predictable when considering the variability in etiology, symptoms ,and treatment results of ADHD. 9

impressively, neither medications responses nor side effects were speculated by ADHD subtype, studies revealed that the advantage of  EEG as a predictor of results outcome rather than as a diagnostic tool. 10

This study designed to assess the presence of EEG changes in children diagnosed with ADHD in order to evaluate role of Antiepileptics compared to Atomoxetine and Antipsychotics.

PATIENTS AND METHODS

Study design

This follow-up study was conducted on 60 Non-epileptic ADHD children aged (6-18) years old attending for treatment to Neuropsychiatry clinic of Police Academy Hospital at Cairo, Egypt from September 2018 to January 2021. the Ethical committee of Al-Azhar Faculty Of Medicine approved this study.

 All children were clinically interviewed semi structurally and were excluded from any other neuropsychiatric or medical disorder, After explaining Aim of our study and verbal consent was obtained.

Procedures

All study children have been diagnosed with ADHD according to the DSM IV criteria SCID, Conner's scale for ADHD was applied for all the study's children.

EEG was obtained for all the children in the study before given treatment and after stabilization of the medications.

Applying medical treatment for all the children and follow up their improvement who categorized into 3 groups, the  first group consists of  27 newly diagnosed children with ADHD with no EEG abnormalities and were given Atomoxetine only regardless of the ADHD type.

While the second group consists of  27 newly diagnosed children with ADHD with no EEG abnormalities and were given a combination of Atomoxetine and Antipsychotic regardless of the ADHD type.

The third group consists of  6 newly diagnosed children with ADHD who have EEG abnormalities and were given only Antiepileptic regardless of ADHD type.

Statistical analysis

We used SPSS version 20.0. qualitative data were described using numbers and percent, the significance of the obtained results was judged at the 5% level.

RESULTS

The Study applied to 60 child diagnosed with ADHD, 70% of them was less than 8 years old, 71.7% are males and 28.3%  are females, 53.3% live in rural areas.

ADHD combined type was predominance type according to the study statistical with 56.7%, ADHD predominance Co-morbid disorder was oppositional defiant disorder ODD.

The Study shows a high statistical significance between ADHD combined type and their educational level (P value<0.001) table 1.


 

Hyperactivityand Attention deficit

p

 

Hyperactivity
(n = 18)

Attention defici
(n= 8)

Both on same degree(n = 34)

 

No.

%

No.

%

No.

%

Age (years)

 

 

 

 

 

 

 

 

From 13 to 18 years

0

0.0

0

0.0

6

17.6

6.658

MCp=
0.117

From 8 to 13 years

2

11.1

3

37.5

7

20.6

Less than 8 years

16

88.9

5

62.5

21

61.8

Gender

 

 

 

 

 

 

 

 

Female

3

16.7

2

25.0

12

35.3

2.062

0.357

Male

15

83.3

6

75.0

22

64.7

Residence

 

 

 

 

 

 

 

 

Urban

13

72.2

8

100.0

7

20.6

23.957*

MCp
<0.001*

Rural

5

27.8

0

0.0

27

79.4

Education

 

 

 

 

 

 

 

 

Above average

10

55.6

0

0.0

0

0.0

56.221*

MCp
<0.001*

Average

3

16.7

8

100.0

1

2.9

Below average

5

27.8

0

0.0

33

97.1

Table 1: Relation between Attention deficit and Hyperactivity and demographic data.

 

 

High statistical significance was found between Co-morbid disorders and male ADHD children (P< 0.005) table 2, and age less than 8 years old (P=0.026) table 2.

 

Comorbid disorder

p

 

No
(n = 10)

conducted
(n= 20)

ODD
(n = 30)

 

No.

%

No.

%

No.

%

Age (years)

 

 

 

 

 

 

 

 

From 13 to 18 years

0

0.0

0

0.0

6

20.0

9.979*

MCp=
0.026*

From 8 to 13 years

0

0.0

4

20.0

8

26.7

Less than 8 years

10

100.0

16

80.0

16

53.3

Gender

 

 

 

 

 

 

 

 

Female

0

0.0

3

15.0

14

46.7

10.670*

0.005*

Male

10

100.0

17

85.0

16

53.3

Residence

 

 

 

 

 

 

 

 

Urban

6

60.0

11

55.0

11

36.7

2.472

0.290

Rural

4

40.0

9

45.0

19

63.3

Education

 

 

 

 

 

 

 

 

Above average

5

50.0

4

20.0

1

3.3

12.173*

MCp=
0.009*

Average

0

0.0

5

25.0

7

23.3

Below average

5

50.0

11

55.0

22

73.3

Table 2 : Relation between co morbid disorder and demographic data.

EEG abnormalities in the Non-epileptic ADHD children of the study were only 10%, with no statistical relationship between them. table 3

While it was obvious according to the study the strong relation between the ADHD children regardless of their types and the Co-morbid disorders with them (P<0.007) table 3.

 

Hyperactivity and Attention deficit

MCp

 

Hyperactivity
(n = 18)

Attention deficit
(n= 8)

Both on same degree(n = 34)

 

No.

%

No.

%

No.

%

EEG

 

 

 

 

 

 

 

 

Changes

1

5.6

2

25.0

3

8.8

2.357

0.307

Normal

17

94.4

6

75.0

31

91.2

Co morbid disorder

 

 

 

 

 

 

 

 

No

5

27.8

0

0.0

5

14.7

13.003*

0.007*

Conducted

10

55.6

3

37.5

7

20.6

ODD

3

16.7

5

62.5

22

64.7

Table 3 :  Relation between Attention deficit and Hyperactivity with EEG and co morbid disorder

Study analysis showed a highly statistical significance for ADHD children regardless of their type with their improvement on treatment.(P<0.001) table 4.

As well as the study showed a highly statistical relation between ADHD  hyperactivity type children's improvement when given Atomoxetine\Antipsychotic combination. (P=0.001) table4.

In addition,there was a highly statistical relation between the ADHD combined type children improvement when given  Atomoxetine\Antipsychotic combination.(P=0.010) table 4.

Hyperactivity and Attention deficit

Atomoxetine

Anti-psychotic + Atomoxetine

Anti-epileptic

2

MCp

No.

%

No.

%

No.

%

Overall

12/27

44.4

24/27

88.9

1/6

16.7

17.417*

<0.001*

Hyperactivity

2/9

22.2

9/9

100.0

1/2

50.0

12.021

0.001*

Attention deficit

4/4

100.0

3/4

75.0

0/2

0.0

5.085

0.135

Both on same degree

6/14

42.9

12/14

85.7

0/2

0.0

8.123*

0.010*

Table 4: Comparison between Atomoxetine, Anti-psychotic + Atomoxetine and Anti-epileptic according to Attention deficit and Hyperactivity.

 

 

DISCUSSION

In this study we demonstrate whether Non-epileptic ADHD children are related to any abnormalities of their EEG or not, also we made a follow-up study according to the treatment of all types of ADHD by using Atomoxetine,Atomoxetine\Antipsychotic combination ,and Antiepileptic.

This study was applied to 60 newly diagnosed ADHD who have no previous history of epilepsy.

Study results showed that the ADHD combined type was the predominance type with 56.7%,these findings were corresponding to Socanski study which revealed that the ADHD combined type was predominant in his study. 11

The Current study showed no statistically significant relation between ADHD children regarding their EEG results,as shown there was only 10% with EEG abnormalities,these findings were in agreement with Castaneda-Cabrero's study which found that EEG abnormalities were only in 40% of  the  ADHD study patients . 12

In addition,current study results were in harmony to Silverstri's study which found the EEG abnormalities in non-epileptic ADHD was only 53% in his study group. 13

According to the study,ODD was the predominant ADHD Co-morbid disorder with 50% and these findings consist with Steinhausen study who found that ODD is the most common Comorbidity with ADHD which occurring in 30-67% of youth with ADHD. 14

Also,there was a highly statistical relation between ADHD children and their residency,as the study found that ADHD combined type was more common in rural areas with 79.4% rather than those lives in urban areas, these findings were in harmony with those reported by Willcutt EG who found that the ADHD combined type was 48% of total cases in his study lives in rural areas. 15

The Current study also revealed that there was a highly statistically significant relation between Co-morbid disorders and ADHD children's age as it's more common in ADHD children less than 8 years old, these findings are corresponding to Masi's study which found out that more than 2/3 of ADHD children have a Co-morbid disorder is during early childhood. 16

According to the treatment a Follow-up study was conducted and we found that in the first group of 27 patients who were given only Atomoxetine regardless of ADHD type, improvement was noticed in all patients with ADHD inattention variant 100%,only 22.2% improved from the ADHD  hyperactivity variant and 42.9% improved from the ADHD combined variant. These findings suggest that Atomoxetine has a superior efficacy on ADHD inattention variant rather than ADHD hyperactivity variant. These findings were consistent with Vinutha and her colleague's study which revealed to the superior efficacy of Atomoxetine is significant on inattention more than hyperactivity/impulsivity. 17

While the second group of 27 patients in the current study were given a combination of Atomoxetine\Antipsychotic regardless of ADHD type, improvement was noticed in all patients with ADHD hyperactivity variants 100%,75% improved from the ADHD inattention variant and 85.7% improved from the ADHD combined variant. These findings suggest that Antipsychotic is very effective in controlling ADHD different variants and has a superior efficacy on ADHD hyperactivity variant. these findings are in agreement with many studies which revealed the great efficacy of Antipsychotics on agitation, over activity, aggression, and impulsivity in all their study groups. 18,19

The third group 6 ADHD  patients who showed EEG abnormalities and have NO previous history for epilepsy were given only Antiepileptic, improvement was very frustrating as there was NO noticeable improvement 16.7% in all ADHD regardless of the variant. These findings suggest that there is no relation between Non-epileptic ADHD and their EEG abnormalities, these findings are corresponding to other many studies which revealed that it's not recommended to prescribe Antiepileptic ADHD children with no seizures while stimulants appear to be more effective for the treatment of ADHD. 20

 In addition to PliszkaSstudy which was consistent was the current study findings that there's no role for Antiepileptic as a treatment to ADHD children with no seizures history and should start a trial of a stimulant, if not effective then alternative stimulant used next and if stimulant is not effective or cause intolerable side effects should start with Non-stimulants. 21

Upon the current study,Non-epileptic ADHD children with EEG abnormalities after being given Antiepileptic and repeat EEG still changes are the same, these findings suggest that EEG changes in Non-epileptic ADHD children are strongly related to epilepsy not to the ADHD itself. This is in harmony with K.osamu's study which found out that EEG changes in ADHD are strongly related to epilepsy and shouldn't be referred as ADHD. 22

CONCLUSION

There was a weak correlation of EEG changes and diagnosis of ADHD in children, beside that there was a weak role of Antiepileptic compared to other drugs.

1. Howard B Abikoff , Benedetto Vitiello, Mark A Riddle, Charles   Cunningham, Laurence L Greenhill, James M Swanson, Shirley Z Chuang, Mark Davies, Elizabeth Kastelic, Sharon B Wigal, Lori Evans, Jaswinder K Ghuman, Scott H Kollins, James T McCracken, James J McGough, Desiree W Murray, Kelly Posner, Anne M Skrobala, Tim Wigal . Methylphenidate effects on functional outcomes in the Preschoolers with Attention-Deficit/Hyperactivity Disorder Treatment Study (PATS). Child Adolesc Psychopharmacol.2007 Oct;17(5):581-92..  doi: 10.1089/cap.2007.0068

2 . Soly Erlandsson , Professor,Linda Lundin , PhD &Elisabeth Punzi , PhD. A discursive analysis concerning information on “ADHD” presented to parents by the National Institute of Mental Health (USA) . https://doi.org/10.3402/qhw.v11.30938. Article: 30938 | Accepted 02 Mar 2016, Published online: 05 Apr 2016

3.   Trond Sand , Noralv Breivik, Anita Herigstad . Assessment of ADHD with EEG. 2013 Feb 5;133(3):312-6. doi: 10.4045/tidsskr.12.0224
4.   Lineu C Fonseca , Gloria M A S Tedrus, Marilia C Bianchini, Talita F Silva. Electroencephalographic alpha reactivity on opening the eyes in children with attention-deficit hyperactivity disorder. 2013 Jan;44(1):53-7. doi: 10.1177/1550059412445659
  5.  Inez Buyck , Jan R Wiersema . Resting electroencephalogram in       attention deficit hyperactivity disorder:developmental course and diagnostic value. 2014 May 30;216(3):391-7.doi: 10.1016/j.psychres.2013.12.055. Epub 2014 Jan 11

6.    Martina D Liechti , Lilian Valko, Ueli C Müller, Mirko Döhnert, Renate Drechsler, Hans-Christoph Steinhausen, Daniel Brandeis. Diagnostic value of resting electroencephalogram in attention-deficit/hyperactivity disorder across the lifespan. 2013 Jan;26(1):135-51.  doi: 10.1007/s10548-012-0258-6. Epub 2012 Oct 9

7. Adam R Clarke , Robert J Barry, Franca E Dupuy, Rory McCarthy, Mark Selikowitz, Stuart J Johnstone. Excess beta activity in the EEG of children with attention-deficit/hyperactivity disorder: a disorder of arousal. 2013 Sep;89(3):314-9.  doi: 10.1016/j.ijpsycho.2013.04.009. Epub 2013 Apr 22

8.  F E Dupuy , A R Clarke , R J Barry , M Selikowitz , R McCarthy . EEG and electrodermal activity in girls with Attention-Deficit/Hyperactivity Disorder. Clin Neurophysiol. 2014 Mar;125(3):491-9.  doi: 10.1016/j.clinph.2013.09.007. Epub 2013 Oct 11

9.  Karen J Mullinger , Jade Havenhand, Richard Bowtell. Identifying the sources of the pulse artefact in EEG recordings made inside an MR scanner. Neuroimage. 2013 May 1;71:75-83.  doi: 10.1016/j.neuroimage.2012.12.070. Epub 2013 Jan 8

10. Adeleh Dehghani Nazhvani , Reza Boostani , Somayeh Afrasiabi, Khadijeh Sadatnezhad. Classification of ADHD and BMD patients using visual evoked potential. Clin Neurol Neurosurg. 2013 Nov;115(11):2329-35.  doi: 10.1016/j.clineuro.2013.08.009. Epub 2013 Sep 1

11. Dobrinko Socanski , Anita Herigstad, Per Hove Thomsen, Aarsland Dag, Tor Ketil Larsen. Epileptiform abnormalities in children diagnosed with attention deficit/hyperactivity disorder. Epilepsy Behav. 2010 Nov;19(3):483-6.  doi: 10.1016/j.yebeh.2010.08.005

12. C Castañeda-Cabrero , G Lorenzo-Sanz, E Caro-Martínez, J M Galán-Sánchez, J Sáez-Alvarez, P Quintana-Aparicio, F Paradinas-Jiménez. Electroencephalographic alterations in children with attention deficit hyperactivity disorder. Rev Neurol. 2003 Nov 16-30;37(10):904-8

13.   Rosalia Silvestri  , Antonella Gagliano , Tiziana Calarese , Irene Aric`o , Clemente Cedro, Rosaria Condurso, Eva German`o , Giuseppe Vita , Gaetano Tortorella. Ictal and interictal EEG abnormalities in ADHD children recorded over night by video-polysomnography. Published by Elsevier B.V. doi:10.1016/j.eplepsyres.2007.05.007

14.   Hans-Christoph Steinhausen , Torunn Stene Nøvik , Gisli Baldursson, Paolo Curatolo, Maria J Lorenzo, Rob Rodrigues Pereira, Stephen J Ralston, Aribert Rothenberger, ADORE Study Group. Co-existing psychiatric problems in ADHD in the ADORE cohort. Eur Child Adolesc Psychiatry. 2006 Dec;15 Suppl 1:I25-9.  doi: 10.1007/s00787-006-1004-y

15.   Erik G. Willcutt. The Prevalence of DSM-IV Attention-Deficit/Hyperactivity Disorder: A Meta-Analytic Review. Neurotherapeutics. 2012 Jul; 9(3): 490–499. Published online 2012 Aug 15. doi: 10.1007/s13311-012-0135-8
16.   Laura Masi MD, Martin Gignac MD. ADHD and Comorbid Disorders in Childhood Psychiatric Problems, Medical Problems, Learning Disorders and Developmental Coordination Disorder. January 2015;Vol.1No1:5 DOI:10.21767/2471-9854.100005

17.   Vinutha Ravishankar , Suresh Vedaveni Chowdappa  , Vivek Benegal , Kesavan Muralidharan . The efficacy of atomoxetine in treating adult attention deficit hyperactivity disorder (ADHD): A meta-analysis of controlled trials. Asian J Psychiatr. 2016 Dec;24:53-58.  doi: 10.1016/j.ajp.2016.08.017. Epub 2016 Aug 25

18.   Mark Olfson , Carlos Blanco, Linxu Liu, Carmen Moreno, Gonzalo Laje. National trends in the outpatient treatment of children and adolescents with antipsychotic drugs. Arch Gen Psychiatry. 2006 Jun;63(6):679-85.  doi: 10.1001/archpsyc.63.6.679

19.   David  Linton , Alasdair  M Barr, William G Honer , Ric M Procyshyn. Antipsychotic and psychostimulant drug combination therapy in attention deficit/hyperactivity and disruptive behavior disorders: a systematic review of efficacy and tolerability. Curr Psychiatry Rep. 2013 May;15(5):355.  doi: 10.1007/s11920-013-0355-6

20. Alcy R Torres , Jane Whitney, Joseph Gonzalez-Heydrich. Attention-deficit/hyperactivity disorder in pediatric patients with epilepsy: review of pharmacological treatment. Epilepsy Behav. 2008 Feb;12(2):217-33.  doi: 10.1016/j.yebeh.2007.08.001. Epub 2007 Dec 11

21.  Steven Pliszka, AACAP Work Group on Quality Issues. Practice parameter for the assessment and treatment of children and adolescents with attention-deficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry. 2007 Jul;46(7):894-921.  doi: 10.1097/chi.0b013e318054e724

1. Howard B Abikoff , Benedetto Vitiello, Mark A Riddle, Charles   Cunningham, Laurence L Greenhill, James M Swanson, Shirley Z Chuang, Mark Davies, Elizabeth Kastelic, Sharon B Wigal, Lori Evans, Jaswinder K Ghuman, Scott H Kollins, James T McCracken, James J McGough, Desiree W Murray, Kelly Posner, Anne M Skrobala, Tim Wigal . Methylphenidate effects on functional outcomes in the Preschoolers with Attention-Deficit/Hyperactivity Disorder Treatment Study (PATS). Child Adolesc Psychopharmacol.2007 Oct;17(5):581-92..  doi: 10.1089/cap.2007.0068

2 . Soly Erlandsson , Professor,Linda Lundin , PhD &Elisabeth Punzi , PhD. A discursive analysis concerning information on “ADHD” presented to parents by the National Institute of Mental Health (USA) . https://doi.org/10.3402/qhw.v11.30938. Article: 30938 | Accepted 02 Mar 2016, Published online: 05 Apr 2016

3.   Trond Sand , Noralv Breivik, Anita Herigstad . Assessment of ADHD with EEG. 2013 Feb 5;133(3):312-6. doi: 10.4045/tidsskr.12.0224
4.   Lineu C Fonseca , Gloria M A S Tedrus, Marilia C Bianchini, Talita F Silva. Electroencephalographic alpha reactivity on opening the eyes in children with attention-deficit hyperactivity disorder. 2013 Jan;44(1):53-7. doi: 10.1177/1550059412445659
  5.  Inez Buyck , Jan R Wiersema . Resting electroencephalogram in       attention deficit hyperactivity disorder:developmental course and diagnostic value. 2014 May 30;216(3):391-7.doi: 10.1016/j.psychres.2013.12.055. Epub 2014 Jan 11

6.    Martina D Liechti , Lilian Valko, Ueli C Müller, Mirko Döhnert, Renate Drechsler, Hans-Christoph Steinhausen, Daniel Brandeis. Diagnostic value of resting electroencephalogram in attention-deficit/hyperactivity disorder across the lifespan. 2013 Jan;26(1):135-51.  doi: 10.1007/s10548-012-0258-6. Epub 2012 Oct 9

7. Adam R Clarke , Robert J Barry, Franca E Dupuy, Rory McCarthy, Mark Selikowitz, Stuart J Johnstone. Excess beta activity in the EEG of children with attention-deficit/hyperactivity disorder: a disorder of arousal. 2013 Sep;89(3):314-9.  doi: 10.1016/j.ijpsycho.2013.04.009. Epub 2013 Apr 22

8.  F E Dupuy , A R Clarke , R J Barry , M Selikowitz , R McCarthy . EEG and electrodermal activity in girls with Attention-Deficit/Hyperactivity Disorder. Clin Neurophysiol. 2014 Mar;125(3):491-9.  doi: 10.1016/j.clinph.2013.09.007. Epub 2013 Oct 11

9.  Karen J Mullinger , Jade Havenhand, Richard Bowtell. Identifying the sources of the pulse artefact in EEG recordings made inside an MR scanner. Neuroimage. 2013 May 1;71:75-83.  doi: 10.1016/j.neuroimage.2012.12.070. Epub 2013 Jan 8

10. Adeleh Dehghani Nazhvani , Reza Boostani , Somayeh Afrasiabi, Khadijeh Sadatnezhad. Classification of ADHD and BMD patients using visual evoked potential. Clin Neurol Neurosurg. 2013 Nov;115(11):2329-35.  doi: 10.1016/j.clineuro.2013.08.009. Epub 2013 Sep 1

11. Dobrinko Socanski , Anita Herigstad, Per Hove Thomsen, Aarsland Dag, Tor Ketil Larsen. Epileptiform abnormalities in children diagnosed with attention deficit/hyperactivity disorder. Epilepsy Behav. 2010 Nov;19(3):483-6.  doi: 10.1016/j.yebeh.2010.08.005

12. C Castañeda-Cabrero , G Lorenzo-Sanz, E Caro-Martínez, J M Galán-Sánchez, J Sáez-Alvarez, P Quintana-Aparicio, F Paradinas-Jiménez. Electroencephalographic alterations in children with attention deficit hyperactivity disorder. Rev Neurol. 2003 Nov 16-30;37(10):904-8

13.   Rosalia Silvestri  , Antonella Gagliano , Tiziana Calarese , Irene Aric`o , Clemente Cedro, Rosaria Condurso, Eva German`o , Giuseppe Vita , Gaetano Tortorella. Ictal and interictal EEG abnormalities in ADHD children recorded over night by video-polysomnography. Published by Elsevier B.V. doi:10.1016/j.eplepsyres.2007.05.007

14.   Hans-Christoph Steinhausen , Torunn Stene Nøvik , Gisli Baldursson, Paolo Curatolo, Maria J Lorenzo, Rob Rodrigues Pereira, Stephen J Ralston, Aribert Rothenberger, ADORE Study Group. Co-existing psychiatric problems in ADHD in the ADORE cohort. Eur Child Adolesc Psychiatry. 2006 Dec;15 Suppl 1:I25-9.  doi: 10.1007/s00787-006-1004-y

15.   Erik G. Willcutt. The Prevalence of DSM-IV Attention-Deficit/Hyperactivity Disorder: A Meta-Analytic Review. Neurotherapeutics. 2012 Jul; 9(3): 490–499. Published online 2012 Aug 15. doi: 10.1007/s13311-012-0135-8
16.   Laura Masi MD, Martin Gignac MD. ADHD and Comorbid Disorders in Childhood Psychiatric Problems, Medical Problems, Learning Disorders and Developmental Coordination Disorder. January 2015;Vol.1No1:5 DOI:10.21767/2471-9854.100005

17.   Vinutha Ravishankar , Suresh Vedaveni Chowdappa  , Vivek Benegal , Kesavan Muralidharan . The efficacy of atomoxetine in treating adult attention deficit hyperactivity disorder (ADHD): A meta-analysis of controlled trials. Asian J Psychiatr. 2016 Dec;24:53-58.  doi: 10.1016/j.ajp.2016.08.017. Epub 2016 Aug 25

18.   Mark Olfson , Carlos Blanco, Linxu Liu, Carmen Moreno, Gonzalo Laje. National trends in the outpatient treatment of children and adolescents with antipsychotic drugs. Arch Gen Psychiatry. 2006 Jun;63(6):679-85.  doi: 10.1001/archpsyc.63.6.679

19.   David  Linton , Alasdair  M Barr, William G Honer , Ric M Procyshyn. Antipsychotic and psychostimulant drug combination therapy in attention deficit/hyperactivity and disruptive behavior disorders: a systematic review of efficacy and tolerability. Curr Psychiatry Rep. 2013 May;15(5):355.  doi: 10.1007/s11920-013-0355-6

20. Alcy R Torres , Jane Whitney, Joseph Gonzalez-Heydrich. Attention-deficit/hyperactivity disorder in pediatric patients with epilepsy: review of pharmacological treatment. Epilepsy Behav. 2008 Feb;12(2):217-33.  doi: 10.1016/j.yebeh.2007.08.001. Epub 2007 Dec 11

21.  Steven Pliszka, AACAP Work Group on Quality Issues. Practice parameter for the assessment and treatment of children and adolescents with attention-deficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry. 2007 Jul;46(7):894-921.  doi: 10.1097/chi.0b013e318054e724

22.   Osamu Kanazawa. Reappraisal of abnormal EEG findings in children with ADHD: on the relationship between ADHD and epileptiform discharges. Epilepsy Behav. 2014 Dec;41:251-6.  doi: 10.1016/j.yebeh.2014.09.078. Epub 2014 Nov 5