Higuchi fractal dimension applied to RR intervals in children with Attention Defi cit Hyperactivity Disorder

Autores

  • Rubens Wajnsztejn Núcleo Especializado em Aprendizagem da Faculdade de Medicina do ABC, FMABC, Santo André, SP
  • Tatiana Dias de Carvalho Departamento de Medicina, Disciplina de Cardiologia, Universidade Federal de São Paulo, UNIFESP, São Paulo/ Laboratório de Delineamento de Estudos e Escri ta Científi ca da Faculdade de Medicina do ABC, FMABC, Santo André, SP.
  • David M. Garner Cardiorespiratory Research Group, Department of Biological and Medical Sciences, Faculty of Health and Life Sciences, Oxford Brookes University
  • Rodrigo Daminello Raimundo Laboratório de Delineamento de Estudos e Escri ta Científi ca da Faculdade de Medicina do ABC, FMABC, Santo André, SP.
  • Luiz Carlos Marques Vanderlei Departamento de Fisioterapia da Faculdade de Ciências e Tecnologia, Universidade Estadual Paulista, UNESP, Presidente Prudente, SP
  • Moacir Fernandes Godoy Núcleo Transdisciplinar de Estudos do Caos e da Complexidade, Faculdade de Medicina de São José de Rio Preto, FAMERP, São José do Rio Preto, SP.
  • Celso Ferreira Departamento de Medicina, Disciplina de Cardiologia, Universidade Federal de São Paulo, UNIFESP, São Paulo, SP
  • Vitor E. Valenti Departamento de Fonoaudiologia da Faculdade de Filosofi a e Ciências, Universidade Estadual Paulista, UNESP, Marília, SP.
  • Luiz Carlos de Abreu Laboratório de Delineamento de Estudos e Escri ta Científi ca da Faculdade de Medicina do ABC, FMABC, Santo André, SP.

DOI:

https://doi.org/10.7322/jhgd.119256

Palavras-chave:

Attention defi cit hyperactivity disorder, Children, Fractal physiology, Heart rate variability, Higuchi fractal dimension.

Resumo

Background: Attention defi cit hyperactivity disorder (ADHD) is categorized by a lowered attention span, recklessness, and hyperactivity. Autonomic nervous system inequality has previously been studied using the same data by chaotic global techniques. We aim to compare the autonomic function of children with ADHD and controls by analyzing heart rate variability (HRV). Methods: 28 children with ADHD (22 boys, mean age 10.0 years ± 1.9 years) and 28 controls (15 boys, mean age 9.9 years ± 1.8 years) rested in supine position with spontaneous breathing for 20 minutes. Heart rate was recorded beat by beat. HRV analysis was performed by Higuchi Fractal Dimension technique. Results: ADHD promoted an increase in the Higuchi Fractal Dimension. The optimum value of Kmax was 10. Conclusion: ADHD signifi cantly altered cardiac autonomic modulation as measured by the Higuchi fractal dimension of HRV. It can therefore be stated that ADHD has increased the complexity of the HRV  signal through cardiac autonomic modulation.

Referências

Tonhajzerova I, Ondrejka I, Adamik P, Hruby R, Javorka M, Trunkvalterova Z, et al. Changes in the cardiac autonomic regulation in children with attention defi cit hyperactivity disorder (ADHD). Indian J Med Res. 2009;130(1):44-50.

Negrao BL, Bipath P, Van der Westhuizen D, Viljoen M. Autonomic correlates at rest and during evoked attention in children with attention-defi cit/hyperactivity disorder and effects of methylphenidate. Neuropsychobiology. 2010;63(2):82-91. DOI: http://dx.doi.org/10.1159/000317548

Meijer WM, Faber A, van den Ban E, Tobi H. Current issues around the pharmacotherapy of ADHD in children and adults. Pharm World Sci. 2009;31(5):509-16. DOI: http://dx.doi.org/10.1007/s11096-009-9302-3

Husarova V, Ondrejka I, Tonhajzerova I. Potential pathomechanisms of ADHD based on neurometabolite changes. Neuro Endocrinol Lett. 2010;31(4):438-45.

Negrao BL, Crafford D, Viljoen M. The effect of sympathomimetic medication on cardiovascular functioning of children with attention-defi cit/hyperactivity disorder: cardiovascular topic. Cardiovascular J Africa. 2009;20(5):296-9.

Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Heart rate variability: standards of measurement, physiological interpretation and clinical use. Circulation. 1996;93(5):1043-65. DOI: http://dx.doi.org/10.1161/01.CIR.93.5.1043

Mackey MC, Milton JG. Dynamical diseases. Ann New York Acad Sci. 1987;504(1):16-32. DOI: http://dx.doi.org/10.1111/j.1749-6632.1987.tb48723.x

Que CL, Kenyon CM, Olivenstein R, Macklem PT, Maksym GN. Homeokinesis and short-term variability of human airway caliber. J Appl Physiol (1985). 2001;91(3):1131-41.

Goldberger AL, Peng CK, Lipsitz LA. What is physiologic complexity and how does it change with aging and disease? Neurobiol Aging. 2002;23(1):23-6.

Goldberger AL, Rigney DR, Mietus J, Antman EM, Greenwald S. Nonlinear dynamics in sudden cardiac death syndrome: heartrate oscillations and bifurcations. Experientia. 1988;44(11-12):983-7.

Skinner JE, Molnar M, Vybiral T, Mitra M. Application of chaos theory to biology and medicine. Integr Physiol Behav Sci. 1992;27(1):39-53.

Stead M, Worrell GA, Litt B. Frequency and dependence of long range temporal correlations in human hippocampal energy fl uctuations. Complexity. 2005;10(5):35-44. DOI: http://dx.doi.org/10.1002/cplx.20088

Ponnusamy A, Marques JL, Reuber M. Comparison of heart rate variability parameters during complex partial seizures and psychogenic nonepileptic seizures. Epilepsia. 2012;53(8):1314-21. DOI: http://dx.doi.org/10.1111/j.1528-1167.2012.03518.x

Ponnusamy A, Marques JL, Reuber M. Heart rate variability measures as biomarkers in patients with psychogenic nonepileptic seizures: potential and limitations. Epilepsy Behav.. 2011;22(4):685-91. DOI: http://dx.doi.org/10.1016/j.yebeh.2011.08.020

Tulppo MP1, Kiviniemi AM, Hautala AJ, Kallio M, Seppänen T, Mäkikallio TH, et al. Physiological background of the loss of fractal heart rate dynamics. Circulation. 2005;112(3):314-19. DOI: http://dx.doi.org/10.1161/CIRCULATIONAHA.104.523712

Seely AJE, Macklem PT. Complex systems and the technology of variability analysis. Crit Care. 2004;8(6):R367-84. DOI: http://dx.doi.org/10.1186/cc2948

Khoa TQD, Ha VQ, Toi VV. Higuchi fractal properties of onset epilepsy electroencephalogram. Computational Mathematical Methods Med. 2012;1-6. DOI: http://dx.doi.org/10.1155/2012/461426

Anier A, Lipping T, Melto S, Hovilehto S. Higuchi fractal dimension and spectral entropy as measures of depth of sedation in intensive care unit. Conf ProcI EEE Eng Med Biol Soc. 2004;1:526-9. DOI: http://dx.doi.org/10.1109/IEMBS.2004.1403210

Higuchi T. Approach to an irregular time series on the basis of the fractal theory. Physica D. 1988;31(2):277-83. DOI: http://dx.doi.org/10.1016/0167-2789(88)90081-4

Skinner JE, Carpeggiani C, Landisman CE, Fulton KW. Correlation dimension of heartbeat intervals is reduced in conscious pigs by myocardial ischemia. Circ Res. 1991;68(4):966-76.

Molnar M, Skinner JE. Correlation dimension changes of the EEG during the wakefulness-sleep cycle. Acta Biochim Biophys Hung. 1991-1992;26(1-4):121-5.

Molnar M, Skinner JE, Csepe V, Winkler I, Karmos G. Correlation dimension changes accompanying the occurrence of the mismatch negativity and the P3 event-related potential component. Electroencephalogr Clin Neurophysiol. 1995;95(2):118-26.

Van Leeuwen P, Bettermann H, An der HU, Kummell HC. Circadian aspects of apparent correlation dimension in human heart rate dynamics. Am J Physiol. 1995;269(1 Pt 2):H130-4.

Kotini A, Anninos P. Detection of non-linearity in schizophrenic patients using magnetoencephalography. Brain Topogr. 2002;15(2):107-13.

Anninos PA, Adamopoulos AV, Kotini A, Tsagas N. Nonlinear analysis of brain activity in magnetic infl uenced Parkinson patients. Brain Topogr. 2000;13(2):135-44.

Babloyantz A, Destexhe A. The Creutzfeld-Jakob disease in the hierarchy of chaotic attractors. In: Markus M, Muller S, Nicolis G. From chemical to biological organization. Springer; 1988. p. 307-16.

Park S, Kim JW, Yang YH, Hong SB, Park MH, Kim BN, et al. Possible effect of norepinephrine transporter polymorphisms on methylphenidate-induced changes in neuropsychological function in attention-defi cit hyperactivity disorder. Behav Brain Funct. 2012;8:22. DOI: : http://dx.doi.org/10.1186/1744-9081-8-22

Cantwell DP. Attention defi cit disorder: a review of the past 10 years. J Am Acad Child Adolesc Psychiatry. 1996;35(8):978-87. DOI: http://dx.doi.org/ 10.1097/00004583-199608000-00008

Lohman TG, Roche AF, Martorell R. Anthropometric standardization reference manual. Champaign; 1988.

Vanderlei LCM, Silva RA, Pastre CM, Azevedo FM, Godoy MF. Comparison of the Polar S810i monitor and the ECG for the analysis of heart rate variability in the time and frequency domains. Braz J Med Biol Res. 2008;41(10):854-9. DOI: http://dx.doi.org/10.1590/S0100-879X2008005000039

Gamelin FX, Baquet G, Berthoin S, Bosquet L. Validity of the polar S810 to measure R-R intervals in children. Int J Sports Med. 2008;29(2):134-8. DOI: http://dx.doi.org/10.1055/s-2007-964995

Gamelin FX, Berthoin S, Bosquet L. Validity of the polar S810 heart rate monitor to measure R-R intervals at rest. Med Sci Sports Exerc.. 2006;38(5):887-93. DOI: http://dx.doi.org/10.1249/01.mss.0000218135.79476.9c

Godoy MF, Takakura IT, Correa PR. Relevância da análise do comportamento dinâmico não linear (Teoria do Caos) como elemento prognóstico de morbidade e mortalidade em pacientes submetidos à cirurgia de revascularização miocárdica. Arq Ciênc Saúde. 2005;12(4):167-71.

Accardo A, Affinito M, Carrozzi M, Bouquet F. Use of the fractal dimension for the analysis of electroencephalographic time series. Biol Cybern. 1997;77(5):339-50. DOI: http://dx.doi.org/10.1007/s004220050394

Ferenets R, Lipping T, Anier A, Jantti V, Melto S, Hovilehto S. Comparison of entropy and complexity measures for the assessment of depth of sedation. IEEE Trans Biomed Eng. 2006;53(6):1067-77. DOI: http://dx.doi.org/10.1109/TBME.2006.873543

Doyle TL, Dugan EL, Humphries B, Newton RU. Discriminating between elderly and young using a fractal dimension analysis of centre of pressure. Int J Med Sci. 2004;1(1):11.

Acharya R, Bhat PS, Kannathal N, Rao A, Lim CM. Analysis of cardiac health using fractal dimension and wavelet transformation. ITBM-RBM. 2005;26(2):133-9. DOI: http://dx.doi.org/10.1016/j.rbmret.2005.02.001

Anderson TW, Darling DA. A test of goodness of fit. J Am Statistical Associat. 1954;49(268):765-9.

Razali NM, Wah YB. Power comparisons of shapiro-wilk, kolmogorov-smirnov, lilliefors and Power comparisons of shapiro-wilk, kolmogorov-smirnov, lilliefors and Anderson-Darling tests. J Statist Modeling Analytics. 2011;2(1):21-33.

Kruskal WH, Wallis WA. Use of ranks in one-criterion variance analysis. J Ame Statist Associat. 1952;260(47):583-621.

de Carvalho TD, Wajnsztejn R, de Abreu LC, Marques Vanderlei LC, Godoy MF, Adami F, et al. Analysis of cardiac autonomic modulation of children with attention defi cit hyperactivity disorder. Neuropsychiatr Dis Treat. 2014;10:613-8. DOI: http://dx.doi.org/10.2147/NDT.S49071

Wajnsztejn R, Carvalho TD, Garner DM, Vanderlei LCM, Godoy MF, Raimundo RD, et al. Heart rate variability analysis by chaotic global techniques in children with attention deficit hyperactivity disorder. Complexity. 2016;21(6):412-19. DOI: http://dx.doi.org/10.1002/cplx.21700

Garner DM, Ling BWK. Measuring and locating zones of chaos and irregularity. J Syst Sci Complexity. 2014;27(3):494-506. DOI: http://dx.doi.org/10.1007/s11424-014-2197-7

Tonhajzerová I, Ondrejka I, Farský I, Višňovcová Z, Mešťaník M, Javorka M, et al. Attention defi cit/hyperactivity disorder (ADHD) is associated with altered heart rate asymmetry. Physiol Res. 2014;63(Suppl 4):S509-19.

Pincus S. Approximate entropy (ApEn) as a complexity measure. Chaos. 1995;5(1):110-7.

Van Leeuwen P1, Cysarz D, Edelhäuser F, Grönemeyer D. Heart rate variability in the individual fetus. Auton Neurosci. 2013;178(1-2):24-8. DOI: http://dx.doi.org/10.1016/j.autneu.2013.01.005

Hornero R, Escudero J, Fernandez A, Poza J, Gomez C. Spectral and nonlinear analyses of MEG background activity in patients with Alzheimer’s disease. IEEE Trans Biomed Eng. 2008;55(6):1658-65.

Lake S. Approximate Entropy and Sample Entropy. [cited 2015 Oct 08] Available from: http://tug.org/pipermail/texhax/attachments/20100616/9225924f/attachment-0007.doc.

Richman JS, Lake DE, Moorman JR. Sample entropy. Methods Enzymol. 2004;384:172-84. DOI: http://dx.doi.org/10.1016/S0076-6879(04)84011-4

Vuksanovic V, Gal V. Nonlinear and chaos characteristics of heart period time series: healthy aging and postural change. Auton Neurosci. 2005;121(1-2):94-100. DOI: http://dx.doi.org/10.1016/j.autneu.2005.06.004

Carvalho TD, Pastre CM, Godoy MF, Ferreira C, Pitta FO, Abreu LC, et al. Fractal correlation property of heart rate variability in chronic obstructive pulmonary disease. Int J Chron Obstruct Pulmon Dis. 2011; 6:23–28. DOI: http://dx.doi.org/10.2147/COPD.S15099

Downloads

Publicado

2016-08-29

Edição

v. 26 n. 2 (2016)

Seção

Artigos Originais

Licença

CODE OF CONDUCT FOR JOURNAL  PUBLISHERS

 

Publishers who are Committee on Publication Ethics members and who support COPE membership for journal editors should:

 

Publishers should:

 

  • Define the relationship between publisher, editor and other parties in a contract
  • Respect privacy (for example, for research participants, for authors, for peer reviewers)
  • Protect intellectual property and copyright
  • Foster editorial independence

 

Publishers should work with journal editors to:

 

  • Set journal policies appropriately and aim to meet those policies, particularly with respect to:

–         Editorial  independence

–         Research ethics, including confidentiality, consent, and the special requirements for human and animal research

–         Authorship

–         Transparency and integrity (for example, conflicts of interest, research funding, reporting standards

–         Peer review and the role of the editorial team beyond that of the journal editor

–         Appeals and complaints

  • Communicate journal policies (for example, to authors, readers, peer reviewers)
  • Review journal policies periodically, particularly with respect to new recommendations from the COPE
  • Code of Conduct for Editors and the COPE Best Practice Guidelines
  • Maintain the integrity of the academic record
  • Assist the parties (for example, institutions, grant funders, governing bodies) responsible for the investigation of suspected research and publication misconduct and, where possible, facilitate in the resolution of these cases
  • Publish corrections, clarifications, and retractions
  • Publish content on a timely basis