Clinical trial NCT06069323: Therapeutic Use of rTMS in Pediatric ASD and ADHD Cohorts
Official title: Therapeutic Use of Repetitive Transcranial Magnetic Stimulation (rTMS) in Pediatric Autism Spectrum Disorder (ASD) and Attention Deficit Hyperactivity Cohorts (ADHD): a Randomized, Sham-controlled Study.
Study type: INTERVENTIONAL
Overall status: RECRUITING
Phase: NA
Conditions: Autism Spectrum Disorder
ADHD
Neurodevelopmental Disorders
Keywords: TMS
NEUROMODULATION
ASD
ADHD
NEUROSTIMULATION
COGNITION
EXECUTIVE FUNCTIONS
DLPFC
Lead sponsor: Ospedali Riuniti di Foggia
Sponsor class: OTHER
First posted: 2023-10-05
Enrollment: 80
Sex: ALL
Minimum age (years): 6
Maximum age (years): 18
Standard ages: CHILD
ADULT
Accepts healthy volunteers: yes
Allocation: RANDOMIZED
Intervention model: PARALLEL
Intervention model description: A double-blind randomized, placebo-controlled study
Primary purpose: TREATMENT

Brief summary: In this interventional, pilot clinical trial investigators will stimulate the dorsolateral prefrontal cortex (DLPFC) in patients with Autism and ADHD. The goal of the study is to improve Cognition and Executive Functions associated with this brain region and, consequently, ameliorate the core symptoms of the disorders.

Specifically, the primary purpose is to establish the efficacy, safety, and tolerability of TMS in pediatric patients with ASD and ADHD. Concurrently, the research aims to uncover the impact of TMS on particular biomarkers associated with the development of these disorders and validate the hypothesis suggesting that the BDNF gene polymorphism (Val66Met) could influence an individual's susceptibility to TMS.

Participants will be randomized into the active group and placebo group, to guarantee a real assessment of the impact of neurostimulation on the cognitive, behavioral, and biochemical parameters. Participants will be asked to complete a neuropsychological evaluation and a biological sample collection before and after TMS treatment, and 1-month post-treatment completion.

Detailed description: BACKGROUND ASD and ADHD are complex neurodevelopmental disorders with increasing prevalence worldwide. The neurobiology of ASD and ADHD reveals a complex picture of altered excitation-inhibition (E/I) balance, aberrant neuronal activity, and disorganization of brain networks. While cognitive and behavioral abnormalities in ASD are related to excessive excitability (due to altered cortex cytoarchitecture), especially at the prefrontal lobes, ADHD patients show reduced activation in the right VLPFC and DLPFC. Neuroinflammation, glutamate imbalance, and kynurenines pathway (KP) dysfunction seem to play a key role in the pathogenesis of these disorders, creating a self-sustaining auto-toxic loop. Treatment options for these disorders are limited, mainly focusing on early behavioral interventions. While for ASD there are no specific pharmacological treatments to address the core symptoms, psychostimulants are considered the most effective therapy for patients with ADHD. Unfortunately, various side effects and the potential for abuse with no reduction in symptom severity in long-term use can restrict its administration. In this scenario, transcranial magnetic stimulation (TMS) could emerge as a reliable therapeutic option. TMS involves magnetic stimulation of the brain to cause long-term changes in excitability and neurochemical activity, healing the key neurobiological alterations described above.

Although shreds of evidence on its potential use in ASD-ADHD treatment, there are still critical challenges that limit its use in clinical practice. One of the big issues is the problem of heterogeneity of the results and the stimulation protocols used in current studies.

Many factors influence the efficacy of TMS, including the stimulation parameters and the functional state of the targeted region during stimulation. Also, the psychotropic drugs taken by enrolled patients may affect TMS outcomes, as they cause long-term changes in synaptic and excitatory balance.

The brain-derived neurotrophic factor (BDNF) gene polymorphism (Val66Met) has been considered a critical contributing factor to individual susceptibility to TMS. BDNF is, indeed involved in early and long-term potentiation, particularly in hippocampal synapses, and its polymorphism has been shown to affect different cognitive functions. According to the most recent data, heterozygous Val/Met individuals were less susceptible to TMS effects.

Finally, another crucial weakness is the lack of longitudinal follow-up, at a well-defined point in time, later neurostimulation. This avoids critical questions regarding possible predictors of outcome (e.g., genetic profiling), length of persistence of benefits, assessing outcome according to the severity of phenotypic presentation, and utility of booster session.

AIMS and OBJECTIVES

The primary aim of the study is to establish the efficacy, safety, and tolerability of TMS in pediatric patients with ASD and ADHD. Key objectives include:

1. Evaluating TMS impact on core symptoms, cognition, and executive functions.
2. Analyzing changes in peripheral biomarkers, such as neurotransmitters, kynurenines, and neurotrophins following TMS.
3. Investigating the role of BDNF gene polymorphism (Val66Met) in TMS individual susceptibility.
4. Identifying clinical profiles and individual factors influencing TMS efficacy (such as cognitive level, ongoing therapies, age, sex, neuropsychiatric comorbidities, clinical severity, etc.).
5. Establishing a longitudinal follow-up to assess predictors of outcome, persistence of benefits, and the utility of booster sessions.

METHODOLOGY It is expected to recruit for this study at least 80 children, divided into 2 groups: 40 children with ASD, and 40 children with ADHD, both of them will be randomly divided into the active group (real TMS stimulation) and the Sham group (placebo stimulation). In case of the inferiority of the sample, due to the difficulty of recruitment, investigators will proceed to administer the active and sham stimulation to the same patients, alternatively, in two different moments, after a proper wash-out. It has been proposed 36-40 months to complete the whole study.

Recruitment of participants will be carried out at the Neuropsychiatry Unit for Children and Adolescents, General Hospital "Riuniti" of Foggia. It has been planned to identify children among hospitalized patients who need a first diagnosis of ADHD and ASD or who need to be followed up. Written informed consent will then be requested from parents, legal tutors, and children wherever possible.

* Study Assessment

This study will be articulated according to the following phases:

1. Collecting and managing biomaterials Peripheral blood, saliva, and urine samples will be collected before and after neurostimulation.

   To verify the impact of TMS on serum and molecular profile in children with neurodevelopmental disorders, we will provide a third biological sample, one month after the last neurostimulation session.

   The following biomarkers will be assessed:

   • Tryptophan and its catabolites: KINA, QUIN, 3-HK, etc.

   • Glutamate, GABA (γ-Aminobutyric acid), Serotonin, and Dopamine.
   * Plasmatic BDNF
   * Inflammatory biomarkers: cortisol, IL-6, IL-1β, TNF-α, TSH, FT3, FT4, Protein-C-reactive (PCR), ferritin.

   A small amount of blood will be used to genotype BDNF gene polymorphism (Val66Met).
2. Clinical and Neuropsychological assessment

   Parents will be asked to complete a set of questionnaires and interview measures designed to assess symptoms of ASD and ADHD, such as:

   • Vineland Adaptive Behavior Scales - Second Edition.

   • Conners 3

   • The Child Behavior Checklist (CBCL).

   • Autism Diagnostic Interview-Revised (ADI-R)

   • Social Communication Questionnaire (SCQ).

   Participants will be asked to complete a battery of cognitive, neuropsychological, and play-based assessments, including:

   • Autism Diagnostic Observation Schedule-2 (ADOS-2).
   * Wechsler Intelligence Scale for Children IV Ed.
   * Leiter International Performance Scale-Revised.
   * Developmental Neuropsychological Assessment, second edition (NEPSY-II)
   * M-ABC (Movement Assessment Battery for Children)
   * Children's Depression Inventory 2™ (CDI 2)
   * Multidimensional Anxiety Scale for Children Second Edition™ (MASC 2)

   Neuropsychological evaluation will be conducted at three different moments, before and after the neurostimulation and 1 month after the last stimulation.
3. EEG data collection and Neurostimulation The Department of Clinical and Experimental Medicine-University of Foggia will perform TMS neurostimulation.

For all participants (both active and sham groups), EEG data will be recorded two times, 30 min before TMS and within 30 min after the last stimulation. The participants will sit in a quiet room, awake and relaxed, with their eyes open. During the data-recording process, 5-10 minutes of resting-state EEG data will be recorded from 32 electrodes positioned according to the 10-10 International System (BrainVision, Brain Products GmbH, Germany).

Matlab and the package EEG lab will be used for offline data analysis.

TMS parameters will be tailored to each disorder's neurobiology. - ASD Protocol The Casanova-Sokhadze research group's TMS protocol will be used because it is the most widely replicated protocol in the pediatric population, with good safety and tolerability as well as fair efficacy.

For repetitive TMS administration, we will use a Magstim R2 stimulator (Magstim Co, UK) with a 70-mm wingspan figure-eight coil, handle oriented approximately 45° from the midline. The neuronavigation system will be utilized to correctly identify the stimulation site (PFC/DLPFC) for every subject. Since it is difficult to treat patients with autism, to avoid their discomfort researchers hypothesize establishing the location of TMS stimulation, through the use of anatomical landmarks corresponding to the scalp regions used for F3 and F4 EEG electrode placement in the 10-20 international system.

Individual MT will be assessed for each hemisphere at the beginning of treatment (L DLPFC, R DLPFC, L + R DLPFC).

Participants will receive 18 rTMS treatment with Fig8 coil twice weekly (9 weeks). The rTMS will be administered with the following stimulation parameters: 1Hz frequency, 90% MT, 180 pulses per session with 9 trains of 20 pulses each with 20-30s intervals between the trains. The initial 6 times, rTMS sessions will be administered over the left DLPFC, followed by 6 sessions targeting the right DLPFC, and an additional 6 treatments will be done bilaterally. The sham rTMS group will receive the same process but the figure-eight coil will be placed vertically on the scalp with no magnetic field penetrated through the skull. The stimulation parameters will be the same as those of the real rTMS. The environmental conditions will be the same for each test (comfortable armchair, quiet room, elbow positioned at 90◦ flexion). Participants will be required to use earplugs during TMS sessions.

The selection of 90% of the Motor Threshold (MT) has been chosen as a precautionary measure to reduce the risk of seizure in this study population, while the choice of 1 Hz of stimulation is based on the evidence that low-frequency improves cortex E/I imbalance.

- ADHD protocol Participants will receive 18 rTMS treatments with Fig-8 coil twice per week (9 weeks). The rTMS will be administered with the following stimulation parameters: 5 (or 10) Hz frequency, 90% MT, 180 pulses per session with 9 trains of 20 pulses each with 20-30 s intervals between the trains. The initial six times, rTMS sessions will be administered over the left DLPFC, followed by 6 sessions targeting the right DLPFC, and an additional 6 treatments will be done bilaterally (over the left and right DLPFC). For the sham rTMS group, the coil will be simply placed perpendicular to the scalp of the stimulation site. The stimulation parameters will be the same as those of the real rTMS.

Studies on children and adolescents with ADHD are significantly fewer than those with ASD. So it is difficult to find a validated and often replicated TMS protocol. For the ADHD population, high-frequency stimulation will be used since it was noted that high frequency can significantly improve ADHD symptoms. It has been also shown that TMS might produce a similar effect on the dopamine system as D-amphetamine a well-known psychostimulant. It has been decided to select 90% of the MT to avoid seizure risk to patients.

At the end of every single session, a questionnaire regarding side effects will be administered to all participants.

BENEFITS AND IMPLICATIONS The study aims to establish a standardized TMS protocol for pediatric ASD and ADHD, addressing heterogeneity in methodology and outcomes.

Since it has been demonstrated that younger age is a predictor of better response to TMS therapy (as children's brains are more plastic than adults), intervening in the pediatric population might result in more effective effects.

Insights into neurotransmitter and biochemical modulation, BDNF's role, and TMS susceptibility can guide personalized interventions. The research could modernize treatment approaches, offering a noninvasive, targeted therapy for these complex disorders. Additionally, the study might identify potential biomarkers for diagnostic and therapeutic purposes.

ETHICAL CONSIDERATIONS AND CONFIDENTIALITY The study has received ethical approval and complies with the Declaration of Helsinki. Personal data will be securely stored, anonymized, and accessible only to authorized personnel. Stringent measures will be taken to ensure participant confidentiality throughout the study.

Eligibility criteria: Inclusion Criteria:

* Patients must have received a diagnosis of "ASD" or "ADHD" according to the Diagnostic and Statistical Manual of Mental Disorder-Fifth edition.
* Patients must be older than 6-7 years of age, to obtain their collaboration easily

Exclusion Criteria:

* presence of known neurological or genetic conditions that are known to affect brain function and structure (i.e. brain tumors, X-fragile, tuberous sclerosis, etc.).
* prescription of psychoactive medication(s) less than 4 weeks prior to joining the study.
* medical history of head trauma associated with prolonged loss of consciousness.
* presence of epilepsy, or history of previous epilepsy, seizures, and repeated febrile seizures.
* presence of comorbidity with psychosis disorder.
* presence of known endocrine, cardiovascular, pulmonary, liver, kidney, or other medical diseases.
* vision and auditory impairment.
* presence of diagnosed chronic or acute inflammation and/or infection.
* lack of consent.

Primary outcomes:
measure: Determining the impact of rTMS on Cognitive Functioning in Real Groups versus Sham Groups, through changes in scores of NEPSY-II sub-scales
timeFrame: Baseline; Post rTMS (9 weeks after baseline); One month follow-up (4 weeks after rTMS)
measure: Determining the impact of rTMS on Depression in Real Groups vs. Sham Groups, through changes in CDI and MASC scores
timeFrame: Baseline; Post rTMS (9 weeks after baseline); One month follow-up (4 weeks after rTMS)
measure: Determining the impact of rTMS on Motor Skills and Coordination in Real Groups vs. Sham Groups, through changes in M-ABC scores
timeFrame: Baseline; Post rTMS (9 weeks after baseline); One month follow-up (4 weeks after rTMS)
measure: Determining the impact of rTMS on Emotional and Behavioral Problems in Real Groups vs. Sham Groups, through changes in CBCL scores
timeFrame: Baseline; Post rTMS (9 weeks after baseline); One month follow-up (4 weeks after rTMS)
measure: Determining the impact of rTMS on Adaptive Behaviors in Real Groups vs. Sham Groups, through changes in Vineland Scale scores
timeFrame: Baseline; Post rTMS (9 weeks after baseline); One month follow-up (4 weeks after rTMS)
measure: Determining the impact of rTMS on ADHD symptoms in Real Groups vs. Sham Groups, through changes in Conners scores
timeFrame: Baseline; Post rTMS (9 weeks after baseline); One month follow-up (4 weeks after rTMS)
measure: Determining the impact of rTMS on Anxiety in Real Groups vs. Sham
timeFrame: Baseline; Post rTMS (9 weeks after baseline); One month follow-up (4 weeks after rTMS)
Secondary outcomes:
measure: Determining the impact of rTMS on BDNF in Real Groups vs. Sham Groups, through changes in BDNF serum concentration.
timeFrame: Baseline; Post rTMS (9 weeks after baseline); One month follow-up (4 weeks after rTMS)
measure: Determining the impact of rTMS on GABA in Real Groups vs. Sham Groups, through changes in serum concentration.
timeFrame: Baseline; Post rTMS (9 weeks after baseline); One month follow-up (4 weeks after rTMS)
measure: Determining the impact of rTMS on glutamate in Real Groups vs. Sham Groups, through changes in serum concentration.
timeFrame: Baseline; Post rTMS (9 weeks after baseline); One month follow-up (4 weeks after rTMS)
measure: Determining the impact of rTMS on dopamine in Real Groups vs. Sham Groups, through changes in serum concentration.
timeFrame: Baseline; Post rTMS (9 weeks after baseline); One month follow-up (4 weeks after rTMS)
measure: Determining the impact of rTMS on serotonin in Real Groups vs. Sham Groups, through changes in serum concentration.
timeFrame: Baseline; Post rTMS (9 weeks after baseline); One month follow-up (4 weeks after rTMS)
measure: Determining the impact of rTMS on Kynurenines Pathway in Real Groups vs. Sham Groups, through changes in kynurenines serum and urine concentration.
timeFrame: Baseline; Post rTMS (9 weeks after baseline); One month follow-up (4 weeks after rTMS)
measure: Determining the impact of rTMS on inflammatory protein IL-1 in Real Groups vs. Sham Groups, through changes in serum concentration.
timeFrame: Baseline; Post rTMS (9 weeks after baseline); One month follow-up (4 weeks after rTMS)
measure: Determining the impact of rTMS on inflammatory protein IL-6 in Real Groups vs. Sham Groups, through changes in serum concentration.
timeFrame: Baseline; Post rTMS (9 weeks after baseline); One month follow-up (4 weeks after rTMS)
measure: Determining the impact of rTMS on inflammatory protein TNF-a in Real Groups vs. Sham Groups, through changes in serum concentration.
timeFrame: Baseline; Post rTMS (9 weeks after baseline); One month follow-up (4 weeks after rTMS)
measure: Determining the impact of rTMS on inflammatory protein CRP (c-reactive protein) in Real Groups vs. Sham Groups, through changes in serum concentration.
timeFrame: Baseline; Post rTMS (9 weeks after baseline); One month follow-up (4 weeks after rTMS)
measure: Determining the impact of rTMS on cortisol in Real Groups vs. Sham Groups, through changes in serum and saliva concentration.
timeFrame: Baseline; Post rTMS (9 weeks after baseline); One month follow-up (4 weeks after rTMS)
Other outcomes:
measure: Determining the impact of rTMS on Event-related potentials (ERPs) in Real Groups vs. Sham Groups, and intra-groups
timeFrame: Baseline; Post rTMS (9 weeks after baseline); One month follow-up (4 weeks after rTMS)
measure: Determining the impact of rTMS on Resting State-EEG in Real Groups vs. Sham Groups, and intra-groups
timeFrame: Baseline; Post rTMS (9 weeks after baseline); One month follow-up (4 weeks after rTMS)
Locations:
city: Foggia
country: Italy
facility: Neuropsychiatric Unit for Child and Adolescent, at General Hospital "Riuniti" of Foggia, University of Foggia
Study officials:
affiliation: Neuropsychiatric Unit for Child and Adolescent, at General Hospital "Riuniti" of Foggia
name: Anna N Polito, MD
role: STUDY_CHAIR
References:
citation: Casanova MF, Buxhoeveden D, Gomez J. Disruption in the inhibitory architecture of the cell minicolumn: implications for autism. Neuroscientist. 2003 Dec;9(6):496-507. doi: 10.1177/1073858403253552.
citation: Casanova MF, Sokhadze EM, Casanova EL, Li X. Transcranial Magnetic Stimulation in Autism Spectrum Disorders: Neuropathological Underpinnings and Clinical Correlations. Semin Pediatr Neurol. 2020 Oct;35:100832. doi: 10.1016/j.spen.2020.100832. Epub 2020 Jun 24.
citation: Hart H, Radua J, Nakao T, Mataix-Cols D, Rubia K. Meta-analysis of functional magnetic resonance imaging studies of inhibition and attention in attention-deficit/hyperactivity disorder: exploring task-specific, stimulant medication, and age effects. JAMA Psychiatry. 2013 Feb;70(2):185-98. doi: 10.1001/jamapsychiatry.2013.277.
citation: Norman LJ, Carlisi C, Lukito S, Hart H, Mataix-Cols D, Radua J, Rubia K. Structural and Functional Brain Abnormalities in Attention-Deficit/Hyperactivity Disorder and Obsessive-Compulsive Disorder: A Comparative Meta-analysis. JAMA Psychiatry. 2016 Aug 1;73(8):815-825. doi: 10.1001/jamapsychiatry.2016.0700.
citation: Rubio B, Boes AD, Laganiere S, Rotenberg A, Jeurissen D, Pascual-Leone A. Noninvasive Brain Stimulation in Pediatric Attention-Deficit Hyperactivity Disorder (ADHD): A Review. J Child Neurol. 2016 May;31(6):784-96. doi: 10.1177/0883073815615672. Epub 2015 Dec 10.
citation: Anderson G, Maes M. Interactions of Tryptophan and Its Catabolites With Melatonin and the Alpha 7 Nicotinic Receptor in Central Nervous System and Psychiatric Disorders: Role of the Aryl Hydrocarbon Receptor and Direct Mitochondria Regulation. Int J Tryptophan Res. 2017 Feb 16;10:1178646917691738. doi: 10.1177/1178646917691738. eCollection 2017.
citation: Savino R, Carotenuto M, Polito AN, Di Noia S, Albenzio M, Scarinci A, Ambrosi A, Sessa F, Tartaglia N, Messina G. Analyzing the Potential Biological Determinants of Autism Spectrum Disorder: From Neuroinflammation to the Kynurenine Pathway. Brain Sci. 2020 Sep 11;10(9):631. doi: 10.3390/brainsci10090631.
citation: Lim CK, Essa MM, de Paula Martins R, Lovejoy DB, Bilgin AA, Waly MI, Al-Farsi YM, Al-Sharbati M, Al-Shaffae MA, Guillemin GJ. Altered kynurenine pathway metabolism in autism: Implication for immune-induced glutamatergic activity. Autism Res. 2016 Jun;9(6):621-31. doi: 10.1002/aur.1565. Epub 2015 Oct 24.
citation: Sathappan AV, Luber BM, Lisanby SH. The Dynamic Duo: Combining noninvasive brain stimulation with cognitive interventions. Prog Neuropsychopharmacol Biol Psychiatry. 2019 Mar 8;89:347-360. doi: 10.1016/j.pnpbp.2018.10.006. Epub 2018 Oct 9.
citation: Cortese S. The neurobiology and genetics of Attention-Deficit/Hyperactivity Disorder (ADHD): what every clinician should know. Eur J Paediatr Neurol. 2012 Sep;16(5):422-33. doi: 10.1016/j.ejpn.2012.01.009. Epub 2012 Feb 2.
citation: Cortese S, Holtmann M, Banaschewski T, Buitelaar J, Coghill D, Danckaerts M, Dittmann RW, Graham J, Taylor E, Sergeant J; European ADHD Guidelines Group. Practitioner review: current best practice in the management of adverse events during treatment with ADHD medications in children and adolescents. J Child Psychol Psychiatry. 2013 Mar;54(3):227-46. doi: 10.1111/jcpp.12036. Epub 2013 Jan 7.
citation: Oberman LM, Enticott PG, Casanova MF, Rotenberg A, Pascual-Leone A, McCracken JT; TMS in ASD Consensus Group. Transcranial magnetic stimulation in autism spectrum disorder: Challenges, promise, and roadmap for future research. Autism Res. 2016 Feb;9(2):184-203. doi: 10.1002/aur.1567. Epub 2015 Nov 4.
citation: Oberman LM, Enticott PG. Editorial: The safety and efficacy of noninvasive brain stimulation in development and neurodevelopmental disorders. Front Hum Neurosci. 2015 Oct 2;9:544. doi: 10.3389/fnhum.2015.00544. eCollection 2015. No abstract available.
citation: Rossi S, Hallett M, Rossini PM, Pascual-Leone A; Safety of TMS Consensus Group. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol. 2009 Dec;120(12):2008-2039. doi: 10.1016/j.clinph.2009.08.016. Epub 2009 Oct 14.
citation: Barahona-Correa JB, Velosa A, Chainho A, Lopes R, Oliveira-Maia AJ. Repetitive Transcranial Magnetic Stimulation for Treatment of Autism Spectrum Disorder: A Systematic Review and Meta-Analysis. Front Integr Neurosci. 2018 Jul 9;12:27. doi: 10.3389/fnint.2018.00027. eCollection 2018.
citation: Sasaki R, Kojima S, Onishi H. Do Brain-Derived Neurotrophic Factor Genetic Polymorphisms Modulate the Efficacy of Motor Cortex Plasticity Induced by Non-invasive Brain Stimulation? A Systematic Review. Front Hum Neurosci. 2021 Sep 28;15:742373. doi: 10.3389/fnhum.2021.742373. eCollection 2021.
citation: Egan MF, Kojima M, Callicott JH, Goldberg TE, Kolachana BS, Bertolino A, Zaitsev E, Gold B, Goldman D, Dean M, Lu B, Weinberger DR. The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell. 2003 Jan 24;112(2):257-69. doi: 10.1016/s0092-8674(03)00035-7.
citation: Blum R, Konnerth A. Neurotrophin-mediated rapid signaling in the central nervous system: mechanisms and functions. Physiology (Bethesda). 2005 Feb;20:70-8. doi: 10.1152/physiol.00042.2004.
citation: Abellaneda-Perez K, Martin-Trias P, Casse-Perrot C, Vaque-Alcazar L, Lanteaume L, Solana E, Babiloni C, Lizio R, Junque C, Bargallo N, Rossini PM, Micallef J, Truillet R, Charles E, Jouve E, Bordet R, Santamaria J, Rossi S, Pascual-Leone A, Blin O, Richardson J, Jovicich J, Bartres-Faz D. BDNF Val66Met gene polymorphism modulates brain activity following rTMS-induced memory impairment. Sci Rep. 2022 Jan 7;12(1):176. doi: 10.1038/s41598-021-04175-x.
citation: Casanova MF, Sokhadze EM, Casanova EL, Opris I, Abujadi C, Marcolin MA, Li X. Translational Neuroscience in Autism: From Neuropathology to Transcranial Magnetic Stimulation Therapies. Psychiatr Clin North Am. 2020 Jun;43(2):229-248. doi: 10.1016/j.psc.2020.02.004. Epub 2020 Apr 8.
citation: Casanova MF, Shaban M, Ghazal M, El-Baz AS, Casanova EL, Sokhadze EM. Ringing Decay of Gamma Oscillations and Transcranial Magnetic Stimulation Therapy in Autism Spectrum Disorder. Appl Psychophysiol Biofeedback. 2021 Jun;46(2):161-173. doi: 10.1007/s10484-021-09509-z.
citation: Casanova MF, Shaban M, Ghazal M, El-Baz AS, Casanova EL, Opris I, Sokhadze EM. Effects of Transcranial Magnetic Stimulation Therapy on Evoked and Induced Gamma Oscillations in Children with Autism Spectrum Disorder. Brain Sci. 2020 Jul 3;10(7):423. doi: 10.3390/brainsci10070423.
citation: Kang J, Zhang Z, Wan L, Casanova MF, Sokhadze EM, Li X. Effects of 1Hz repetitive transcranial magnetic stimulation on autism with intellectual disability: A pilot study. Comput Biol Med. 2022 Feb;141:105167. doi: 10.1016/j.compbiomed.2021.105167. Epub 2021 Dec 23.
citation: Cardullo S, Gomez Perez LJ, Cuppone D, Sarlo M, Cellini N, Terraneo A, Gallimberti L, Madeo G. A Retrospective Comparative Study in Patients With Cocaine Use Disorder Comorbid With Attention Deficit Hyperactivity Disorder Undergoing an rTMS Protocol Treatment. Front Psychiatry. 2021 Mar 25;12:659527. doi: 10.3389/fpsyt.2021.659527. eCollection 2021.
citation: Jannati A, Oberman LM, Rotenberg A, Pascual-Leone A. Assessing the mechanisms of brain plasticity by transcranial magnetic stimulation. Neuropsychopharmacology. 2023 Jan;48(1):191-208. doi: 10.1038/s41386-022-01453-8. Epub 2022 Oct 5.
citation: Giron CG, Lin TTZ, Kan RLD, Zhang BBB, Yau SY, Kranz GS. Non-Invasive Brain Stimulation Effects on Biomarkers of Tryptophan Metabolism: A Scoping Review and Meta-Analysis. Int J Mol Sci. 2022 Aug 26;23(17):9692. doi: 10.3390/ijms23179692.
citation: Regenold WT, Deng ZD, Lisanby SH. Noninvasive neuromodulation of the prefrontal cortex in mental health disorders. Neuropsychopharmacology. 2022 Jan;47(1):361-372. doi: 10.1038/s41386-021-01094-3. Epub 2021 Jul 16.
citation: Lisanby SH. Transcranial Magnetic Stimulation in Psychiatry: Historical Reflections and Future Directions. Biol Psychiatry. 2024 Mar 15;95(6):488-490. doi: 10.1016/j.biopsych.2023.05.001. Epub 2023 May 9. No abstract available.