EEG neurofeedback treatments in children with ADHD: an updated meta-analysis of randomized controlled trials

Jean-Arthur Micoulaud-Franchi, Pierre Alexis Geoffroy, Guillaume Fond, Régis Lopez, Stéphanie Bioulac, Pierre Philip, Jean-Arthur Micoulaud-Franchi, Pierre Alexis Geoffroy, Guillaume Fond, Régis Lopez, Stéphanie Bioulac, Pierre Philip

Abstract

Objective: We undertook a meta-analysis of published Randomized Controlled Trials (RCT) with semi-active control and sham-NF groups to determine whether Electroencephalogram-neurofeedback (EEG-NF) significantly improves the overall symptoms, inattention and hyperactivity/impulsivity dimensions for probably unblinded assessment (parent assessment) and probably blinded assessment (teacher assessment) in children with Attention Deficit Hyperactivity Disorder (ADHD).

Data sources: A systematic review identified independent studies that were eligible for inclusion in a random effects meta-analysis.

Data extraction: Effect sizes for ADHD symptoms were expressed as standardized mean differences (SMD) with 95% confidence intervals.

Results: Five identified studies met eligibility criteria, 263 patients with ADHD were included, 146 patients were trained with EEG-NF. On parent assessment (probably unblinded assessment), the overall ADHD score (SMD = -0.49 [-0.74, -0.24]), the inattention score (SMD = -0.46 [-0.76, -0.15]) and the hyperactivity/impulsivity score (SMD = -0.34 [-0.59, -0.09]) were significantly improved in patients receiving EEG-NF compared to controls. On teacher assessment (probably blinded assessment), only the inattention score was significantly improved in patients receiving EEG-NF compared to controls (SMD = -0.30 [-0.58, -0.03]).

Conclusions: This meta-analysis of EEG-NF in children with ADHD highlights improvement in the inattention dimension of ADHD symptoms. Future investigations should pay greater attention to adequately blinded studies and EEG-NF protocols that carefully control the implementation and embedding of training.

Keywords: attention deficit hyperactivity disorder; learning; neurofeedback; practice guidelines; randomized controlled trial.

Figures

Figure 1
Figure 1
Forest plots with Standardized Mean Difference (SMD), effect size, and homogeneity statistics for the meta-analysis examining total scores of ADHD symptoms, inattention dimension and hyperactivity/Impulsivity dimension assessed by parent (left) and by teacher (right).

References

    1. American Psychiatric Association (2000). Diagnostic and Statistical Manual of Mental Disorder, 4th ed, Text Revision (DSM-IV-TR). Washington, DC: American Psychiatric Association.
    1. Arnold L. E., Lofthouse N., Hersch S., Pan X., Hurt E., Bates B., et al. . (2013). EEG neurofeedback for ADHD: double-blind sham-controlled randomized pilot feasibility trial. J. Atten. Disord. 17, 410–419. 10.1177/1087054712446173
    1. Arns M., de Ridder S., Strehl U., Breteler M., Coenen A. (2009). Efficacy of neurofeedback treatment in ADHD: the effects on inattention, impulsivity and hyperactivity: a meta-analysis. Clin. EEG Neurosci. 40, 180–189. 10.1177/155005940904000311
    1. Arns M., Drinkenburg W., Leon Kenemans J. (2012). The effects of QEEG-informed neurofeedback in ADHD: an open-label pilot study. Appl. Psychophysiol. Biofeedback 37, 171–180. 10.1007/s10484-012-9191-4
    1. Arns M., Heinrich H., Strehl U. (2014). Evaluation of neurofeedback in ADHD: the long and winding road. Biol. Psychol. 95, 108–115. 10.1016/j.biopsycho.2013.11.013
    1. Arns M., Strehl U. (2013). Evidence for efficacy of neurofeedback in ADHD? Am. J. Psychiatry 170, 799–800. 10.1176/appi.ajp.2013.13020208
    1. Bakhshayesh A. R., Hänsch S., Wyschkon A., Rezai M. J., Esser G. (2011). Neurofeedback in ADHD: a single-blind randomized controlled trial. Eur. Child Adolesc. Psychiatry 20, 481–491. 10.1007/s00787-011-0208-y
    1. Bink M., van Nieuwenhuizen C., Popma A., Bongers I. L., van Boxtel G. J. (2014). Neurocognitive effects of neurofeedback in adolescents with ADHD: a randomized controlled trial. J. Clin. Psychiatry 75, 535–542. 10.4088/JCP.13m08590
    1. Borenstein M., Hedges L., Higgins J., Rothstein H. (2009). Introduction to Meta-Analysis. Chichester: Wiley.
    1. Bralten J., Franke B., Waldman I., Rommelse N., Hartman C., Asherson P., et al. . (2013). Candidate genetic pathways for attention-deficit/hyperactivity disorder (ADHD) show association to hyperactive/impulsive symptoms in children with ADHD. J. Am. Acad. Child Adolesc. Psychiatry 52, 1204–1212.e1. 10.1016/j.jaac.2013.08.020
    1. Cannon R. L., Pigott H. E., Surmeli T., Simkin D. R., Thatcher R. W., Van den Bergh W., et al. . (2014). The problem of patient heterogeneity and lack of proper training in a study of EEG neurofeedback in children. J. Clin. Psychiatry 75, 289–290. 10.4088/JCP.13Lr08850
    1. Coben R., Evans J. R. (2011). Neurofeedback and Neuromodulation Techniques and Applications. London: Elsevier.
    1. Dagenais E., Leroux-Boudreault A., El-Baalbaki G., Bégin J. (2014). Doubting the efficacy/effectiveness of electroencephalographic neurofeedback in treating children with attention-deficit/hyperactivity disorder is as yet unjustified. J. Clin. Psychiatry 75, 778–779. 10.4088/JCP.14lr09043
    1. DerSimonian R., Laird N. (1986). Meta-analysis in clinical trials. Control Clin. Trials 7, 177–188. 10.1016/0197-2456(86)90046-2
    1. Duric N. S., Assmus J., Gundersen D., Elgen I. B. (2012). Neurofeedback for the treatment of children and adolescents with ADHD: a randomized and controlled clinical trial using parental reports. BMC Psychiatry 12:107. 10.1186/1471-244X-12-107
    1. Gevensleben H., Holl B., Albrecht B., Schlamp D., Kratz O., Studer P., et al. . (2009a). Distinct EEG effects related to neurofeedback training in children with ADHD: a randomized controlled trial. Int. J. Psychophysiol. 74, 149–157. 10.1016/j.ijpsycho.2009.08.005
    1. Gevensleben H., Holl B., Albrecht B., Vogel C., Schlamp D., Kratz O., et al. . (2009b). Is neurofeedback an efficacious treatment for ADHD? A randomised controlled clinical trial. J. Child Psychol. Psychiatry 50, 780–789. 10.1111/j.1469-7610.2008.02033.x
    1. Gevensleben H., Rothenberger A., Moll G. H., Heinrich H. (2012). Neurofeedback in children with ADHD: validation and challenges. Expert Rev. Neurother. 12, 447–460. 10.1586/ern.12.22
    1. Hedges L., Olkin I. (1985). Statistical Methods for Meta-Analysis. Orlando: Academic Press.
    1. Heinrich H., Gevensleben H., Strehl U. (2007). Annotation: neurofeedback—train your brain to train behaviour. J. Child Psychol. Psychiatry 48, 3–16. 10.1111/j.1469-7610.2006.01665.x
    1. Higgins J. P., Thompson S. G., Deeks J. J., Altman D. G. (2003). Measuring inconsistency in meta-analyses. BMJ 327, 557–560. 10.1136/bmj.327.7414.557
    1. Lansbergen M. M., van Dongen-Boomsma M., Buitelaar J. K., Slaats-Willemse D. (2011). ADHD and EEG-neurofeedback: a double-blind randomized placebo-controlled feasibility study. J. Neural Transm. 118, 275–284. 10.1007/s00702-010-0524-2
    1. Li L., Yang L., Zhuo C. J., Wang Y. F. (2013). A randomised controlled trial of combined EEG feedback and methylphenidate therapy for the treatment of ADHD. Swiss Med. Wkly. 143:w13838. 10.4414/smw.2013.13838
    1. Loo S. K., Teale P. D., Reite M. L. (1999). EEG correlates of methylphenidate response among children with ADHD: a preliminary report. Biol. Psychiatry 45, 1657–1660. 10.1016/s0006-3223(98)00250-9
    1. Maurizio S., Liechti M. D., Heinrich H., Jäncke L., Steinhausen H. C., Walitza S., et al. . (2014). Comparing tomographic EEG neurofeedback and EMG biofeedback in children with attention-deficit/hyperactivity disorder. Biol. Psychol. 95, 31–44. 10.1016/j.biopsycho.2013.10.008
    1. Meisel V., Servera M., Garcia-Banda G., Cardo E., Moreno I. (2014). Reprint of “Neurofeedback and standard pharmacological intervention in ADHD: a randomized controlled trial with six-month follow-up”. Biol. Psychol. 95, 116–125. 10.1016/j.biopsycho.2013.09.009
    1. Micoulaud-Franchi J. A., Quiles C., Fond G., Cermolacce M., Vion-Dury J. (2014). The covariation of independent and dependant variables in neurofeedback: a proposal framework to identify cognitive processes and brain activity variables. Conscious. Cogn. 26, 162–168. 10.1016/j.concog.2014.03.007
    1. Moher D., Liberati A., Tetzlaff J., Altman D. G., PRISMA Group . (2009). Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 6:e1000097. 10.1371/journal.pmed.1000097
    1. Monastra V. J., Lynn S., Linden M., Lubar J. F., Gruzelier J., LaVaque T. J. (2005). Electroencephalographic biofeedback in the treatment of attention-deficit/hyperactivity disorder. Appl. Psychophysiol. Biofeedback 30, 95–114. 10.1007/s10484-005-4305-x
    1. Ogrim G., Hestad K. A. (2013). Effects of neurofeedback versus stimulant medication in attention-deficit/hyperactivity disorder: a randomized pilot study. J. Child Adolesc. Psychopharmacol. 23, 448–457. 10.1089/cap.2012.0090
    1. Polanczyk G., de Lima M. S., Horta B. L., Biederman J., Rohde L. A. (2007). The worldwide prevalence of ADHD: a systematic review and metaregression analysis. Am. J. Psychiatry 164, 942–948. 10.1176/appi.ajp.164.6.942
    1. Poole C. (2001). Low P-values or narrow confidence intervals: which are more durable? Epidemiology 12, 291–294. 10.1097/00001648-200105000-00005
    1. Schwitzgebel R. K., Traugott M. (1968). Initial note on the placebo effect of machines. Behav. Sci. 13, 267–273. 10.1002/bs.3830130402
    1. Sherlin L. H., Arns M., Lubar J., Heinrich H., Kerson C., Strehl U., et al. (2011). Neurofeedback and basic learning therory: implications for research and practice. J. Neurother. 15, 292–304 10.1080/10874208.2011.623089
    1. Sonuga-Barke E., Brandeis D., Cortese S., Daley D., Danckaerts M., Döpfner M., et al. . (2013b). Response to Chronis-Tuscano et al. and Arns and Strehl. Am. J. Psychiatry 170, 800–802. 10.1176/appi.ajp.2013.13020208r
    1. Sonuga-Barke E. J., Brandeis D., Cortese S., Daley D., Ferrin M., Holtmann M., et al. . (2013a). Nonpharmacological interventions for ADHD: systematic review and meta-analyses of randomized controlled trials of dietary and psychological treatments. Am. J. Psychiatry 170, 275–289. 10.1176/appi.ajp.2012.12070991
    1. Steiner N. J., Frenette E. C., Rene K. M., Brennan R. T., Perrin E. C. (2014a). In-school neurofeedback training for ADHD: sustained improvements from a randomized control trial. Pediatrics 133, 483–492. 10.1542/peds.2013-2059d
    1. Steiner N. J., Frenette E. C., Rene K. M., Brennan R. T., Perrin E. C. (2014b). Neurofeedback and cognitive attention training for children with attention-deficit hyperactivity disorder in schools. J. Dev. Behav. Pediatr. 35, 18–27. 10.1097/DBP.0000000000000009
    1. Steiner N. J., Sheldrick R. C., Gotthelf D., Perrin E. C. (2011). Computer-based attention training in the schools for children with attention deficit/hyperactivity disorder: a preliminary trial. Clin. Pediatr. (Phila) 50, 615–622. 10.1177/0009922810397887
    1. Stroebel C. F., Glueck B. C. (1973). Biofeedback treatment in medicine and psychiatry: an ultimate placebo? Semin. Psychiatry 5, 379–393.
    1. The Collaborative Neurofeedback Group. Arnold L. E., Arns M., Conners K., Debeus R., Hirshberg L., et al. . (2013). A proposed multisite double-blind randomized clinical trial of neurofeedback for ADHD: need, rationale and strategy. J. Atten. Disord. 17, 420–436. 10.1177/1087054713482580
    1. van Dongen-Boomsma M. (2014). Dr. van Dongen-Boomsma replies. J. Clin. Psychiatry 75:779. 10.4088/JCP.14lr09043a
    1. van Dongen-Boomsma M., Vollebregt M. A., Slaats-Willemse D., Buitelaar J. K. (2013). A randomized placebo-controlled trial of electroencephalographic (EEG) neurofeedback in children with attention-deficit/hyperactivity disorder. J. Clin. Psychiatry 74, 821–827. 10.4088/JCP.12M08321
    1. van Dongen-Boomsma M., Vollebregt M. A., Slaats-Willemse D., Buitelaar J. K. (2014). Dr van Dongen-Boomsma and colleagues reply. J. Clin. Psychiatry 75:290. 10.4088/JCP.13LR08850a
    1. Vollebregt M. A., van Dongen-Boomsma M., Buitelaar J. K., Slaats-Willemse D. (2014a). Does EEG-neurofeedback improve neurocognitive functioning in children with attention-deficit/hyperactivity disorder? A systematic review and a double-blind placebo-controlled study. J. Child Psychol. Psychiatry 55, 460–472. 10.1111/jcpp.12143
    1. Vollebregt M. A., van Dongen-Boomsma M., Slaats-Willemse D., Buitelaar J. K. (2014b). What future research should bring to help resolving the debate about the efficacy of EEG-neurofeedback in children with ADHD. Front. Hum. Neurosci. 8:321. 10.3389/fnhum.2014.00321

Source: PubMed

Sponsorer og samarbeidspartnere

Medisinsk tilstand

Legemiddelintervensjoner

3
Abonnere