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Investigation of surface electromyography amplitude values during stair climbing task in children with Duchenne muscular dystrophy

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Abstract

Objective

The aims of this study were (a) to examine the surface electromyography (sEMG) amplitude values of the lower limb muscles during stair climbing both between different functional levels of Duchenne muscular dystrophy (DMD), in comparison with healthy children, and (b) to investigate the relationships between sEMG amplitudes and physical performance.

Methods

sEMG amplitudes of the lower limbs of twenty-one children with DMD between levels I and III according to the Brooke Lower Extremity Functional Classification Scale and eleven healthy peers were evaluated by using sEMG during stair climbing task. Physical performance was evaluated by 6-min walk test and ascending 4-step timed performance test.

Results

The lower limb sEMG amplitude values of children with DMD were statistically higher than healthy children (p < 0.001). sEMG amplitudes of the right (p = 0.01) and left (p = 0.003) biceps femoris, the right (p < 0.001) and left (p = 0.001) gastrocnemius medialis, and the right vastus lateralis (p = 0.02) muscles were higher in children with levels 2–3 than those in level 1. Moderate-to-strong relations were found between the gastrocnemius medialis and biceps femoris sEMG amplitudes and physical performance assessments (p < 0.05).

Conclusion

Increased sEMG amplitude values in the lower limbs during stair climbing task are thought to be caused by the effort to compensate for progressive muscle weakness and are associated with lower physical performance in children with DMD. Further, sEMG amplitude values are determined to increase as the functional level deteriorates.

Clinical trial registration number and URL

NCT04287582 (https://clinicaltrials.gov/ct2/show/NCT04287582?term=merve+bora&draw=2&rank=1).

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Data availability

Any data and material associated with this article will be made available by reasonable request to the corresponding author.

Code availability

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References

  1. Bushby K, Finkel R, Birnkrant DJ, Case LE, Clemens PR, Cripe L et al (2010) Diagnosis and management of Duchenne muscular dystrophy, part 1: diagnosis, and pharmacological and psychosocial management. Lancet Neurol 9:77–93. https://doi.org/10.1016/S1474-4422(09)70271-6

    Article  PubMed  Google Scholar 

  2. Emery AE (2002) The muscular dystrophies. Lancet 359(9307):687–695. https://doi.org/10.1016/S0140-6736(02)07815-7

    Article  CAS  PubMed  Google Scholar 

  3. Martini J, Voos MC, Hukuda ME, Resende MB, Caromano FA (2014) Compensatory movements during functional activities in ambulatory children with Duchenne muscular dystrophy. Arq Neuropsiquiatr 72(1):5–11. https://doi.org/10.1590/0004-282X20130196

    Article  PubMed  Google Scholar 

  4. Verma S, Anziska Y, Cracco J (2010) Review of Duchenne muscular dystrophy (DMD) for the pediatricians in the community. Clin Pediatr (Phila) 49(11):1011–1017. https://doi.org/10.1177/0009922810378738

    Article  Google Scholar 

  5. Nadeau S, McFadyen BJ, Malouin F (2003) Frontal and sagittal plane analyses of the stair climbing task in healthy adults aged over 40 years: what are the challenges compared to level walking? Clin Biomech (Bristol, Avon) 18(10):950–959. https://doi.org/10.1016/S0268-0033(03)00179-7

    Article  CAS  Google Scholar 

  6. Bushby K, Finkel R, Birnkrant DJ, Case LE, Clemens PR, Cripe L et al (2010) DMD Care Considerations Working Group. Diagnosis and management of Duchenne muscular dystrophy part 2: implementation of multidisciplinary care. Lancet Neurol 9(2):177–189. https://doi.org/10.1016/S1474-4422(09)70272-8

    Article  CAS  PubMed  Google Scholar 

  7. Natterlund B, Ahlstrom G (2001) Activities of daily living and quality of life in persons with muscular dystrophy. J Rehabil Med 33(5):206–211. https://doi.org/10.1080/165019701750419590

    Article  CAS  PubMed  Google Scholar 

  8. Berard C, Payan C, Hodgkinson I, Fermanian J et al (2005) A motor function measure for neuromuscular diseases. Construction and validation study. Neuromuscul Disord 15(7):463–470. https://doi.org/10.1016/j.nmd.2005.03.004

    Article  PubMed  Google Scholar 

  9. Martini J, Hukuda ME, Caromano FA, Favero FM, Fu C, Voos MC (2015) The clinical relevance of timed motor performance in children with Duchenne muscular dystrophy. Physiother Theory Pract 31(3):173–181. https://doi.org/10.3109/09593985.2014.989294

    Article  PubMed  Google Scholar 

  10. Eteraf Oskouei A, Ferdosrad N, Dianat I, AsghariJafarabadi M, Nazari J (2014) Electromyographic activity of soleus and tibialis anterior muscles during ascending and descending stairs of different heights. Health Promot Perspect 4(2):173–179. https://doi.org/10.5681/hpp.2014.023

    Article  PubMed  PubMed Central  Google Scholar 

  11. Hicks-Little CA, Peindl RD, Hubbard TJ, Scannel BP, Springer BD, Odum SM, Fehring TK, Cordova ML (2011) Lower extremity joint kinematics during stair climbing in knee osteoarthritis. Med Sci Sports Exerc 43(3):516–524. https://doi.org/10.1249/MSS.0b013e3181f257be

    Article  PubMed  Google Scholar 

  12. Spolaor F, Sawacha Z, Guarneri G, Del Din S, Avogaro A, Cobelli C (2016) Altered EMG patterns in diabetic neuropathic and not neuropathic patients during step ascending and descending. J Electromyogr Kinesiol 31:32–39. https://doi.org/10.1016/j.jelekin.2016.08.007

    Article  PubMed  Google Scholar 

  13. Janssen MM, Harlaar J, de Groot IJ (2015) Surface EMG to assess arm function in boys with DMD: a pilot study. J Electromyogr Kinesiol 25(2):323–328. https://doi.org/10.1016/j.jelekin.2015.01.008

    Article  PubMed  Google Scholar 

  14. Lencioni T, Piscosquito G, Rabuffetti M, Sipio ED, Diverio M, Moroni I, Padua L, Pagliano E, Schenone A, Pareyson D, Ferrarin M (2018) Electromyographic and biomechanical analysis of step negotiation in Charcot Marie Tooth subjects whose level walk is not impaired. Gait Posture 62:497–504. https://doi.org/10.1016/j.gaitpost.2018.04.014

    Article  PubMed  Google Scholar 

  15. Matjacic Z, Olensek A, Krajnik J, Eymard B, Zupan A, Praznikar A (2008) Compensatory mechanisms during walking in response to muscle weakness in spinal muscular atrophy, type III. Gait Posture 27(4):661–668. https://doi.org/10.1016/j.gaitpost.2007.08.012

    Article  PubMed  Google Scholar 

  16. Ropars J, Lempereur M, Vuillerot C, Tiffreau V, Peudenier S, Cuisset JM, Pereon Y, Leboeuf F, Delporte L, Delpierre Y, Gross R, Brochard S (2016) Muscle activation during gait in children with Duchenne muscular dystrophy. PLoS ONE 11(9):e0161938. https://doi.org/10.1371/journal.pone.0161938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Sutcu G, Yalcin AI, Ayvat E, OnursalKılınç Ö, Ayvat F, Doğan M, Harput G, Aksu Yıldırım S, Kılınç M (2019) Electromyographic activity and kinematics of sit-to-stand in individuals with muscle disease. Neurol Sci 40(11):2311–2318. https://doi.org/10.1007/s10072-019-03974-5

    Article  PubMed  Google Scholar 

  18. Brooke MH, Griggs RC, Mendell JR, Fenichel GM, Shumate JB, Pellegrino RJ (1981) Clinical trial in Duchenne dystrophy. I. The design of the protocol. Muscle Nerve 4(3):186–197. https://doi.org/10.1002/mus.880040304

    Article  CAS  PubMed  Google Scholar 

  19. Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G (2000) Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol 10(5):361–374. https://doi.org/10.1016/S1050-6411(00)00027-4

    Article  CAS  PubMed  Google Scholar 

  20. - Halaki M, Ginn K (2012) Normalization of EMG signals: to normalize or not to normalize and what to normalize to? Computational intelligence in electromyography analysis-a perspective on current applications and future challenges. Intech. https://doi.org/10.5772/49957

  21. Norton K, Olds T (1996) Anthropometrica. Sydney University of New South Wales Press

  22. Hogrel JY et al (2007) Development of a French isometric strength normative database for adults using quantitative muscle testing. Arch Phys Med Rehabil 88(10):1289–1297. https://doi.org/10.1016/j.apmr.2007.07.011

    Article  PubMed  Google Scholar 

  23. McDonald CM, Henricson EK, Abresch RT, Florence J, Eagle M, Gappmaier E et al (2013) The 6-minute walk test and other clinical endpoints in Duchenne muscular dystrophy: reliability, concurrent validity, and minimal clinically important differences from a multicenter study. Muscle Nerve 48(3):357–368. https://doi.org/10.1002/mus.23905

    Article  PubMed  PubMed Central  Google Scholar 

  24. McDonald CM, Henricson EK, Han JJ, Abresch RT, Nicorici A, Elfring GL, Atkinson L, Reha A, Hirawat S, Miller LL (2010) The 6-minute walk test as a new outcome measure in Duchenne muscular dystrophy. Muscle Nerve 41(4):500–510. https://doi.org/10.1002/mus.21544

    Article  PubMed  Google Scholar 

  25. Overholser B, Sowinski KM (2008) Biostatistics primer: part 2. Nutr Clin Pract 23(1):76–84. https://doi.org/10.1177/011542650802300176

    Article  PubMed  Google Scholar 

  26. Schober P, Boer C, Schwarte LA (2018) Correlation coefficients: appropriate use and interpretation. Anesth Analg 126(5):1763–1768

    Article  Google Scholar 

  27. Esposito F, Ce E, Rampichini S, Monti E, Limonta E, Fossati B et al (2017) Electromechanical delays during a fatiguing exercise and recovery in patients with myotonic dystrophy type 1. Eur J Appl Physiol 117:551–566. https://doi.org/10.1007/s00421-017-3558-4

    Article  PubMed  Google Scholar 

  28. Esposito F, Cè E, Rampichini S, Limonta E, Venturelli M, Monti E, Bet L, Fossati B, Meola G (2016) Electromechanical delay components during skeletal muscle contraction and relaxation in patients with myotonic dystrophy type 1. Neuromuscul Disord 26(1):60–72. https://doi.org/10.1016/j.nmd.2015.09.013

    Article  PubMed  Google Scholar 

  29. Armand S, Mercier M, Watelain E, Patte K, Pelissier J, Rivier F (2005) A comparison of gait in spinal muscular atrophy, type II and Duchenne muscular dystrophy. Gait Posture 21(4):369–378. https://doi.org/10.1016/j.gaitpost.2004.04.006

    Article  PubMed  Google Scholar 

  30. Patte K, Pélissier J, Bénaim C, Laassel EM, Guibal C, Echenne B (2000) Gait analysis in Duchenne muscular dystrophy. Ann Readapt Med Phys 43:53–68. https://doi.org/10.1016/S0168-6054(00)88728-0

    Article  Google Scholar 

  31. Sutherland DH, Olshen R, Cooper L et al (1981) The pathomechanics of gait in Duchenne muscular dystrophy. Dev Med Child Neurol 23:3–22. https://doi.org/10.1111/j.1469-8749.1981.tb08442.x

    Article  CAS  PubMed  Google Scholar 

  32. SelkGhafari A, Meghdari A, Vossoughi GR (2009) Muscle-driven forward dynamics simulation for the study of differences in muscle function during stair ascent and descent. Proc Inst Mech Eng H 223(7):863–874. https://doi.org/10.1243/09544119JEIM578

    Article  CAS  Google Scholar 

  33. West NA, Yang ML, Weitzenkamp DA, Andrews J, Meaney FJ, Oleszek J, Miller LA, Matthews D, DiGuiseppi C (2013) Patterns of growth in ambulatory males with Duchenne muscular dystrophy. J Pediatr 163(6):1759-1763.e1. https://doi.org/10.1016/j.jpeds.2013.08.004

    Article  PubMed  Google Scholar 

  34. Baptista CR, Costa AA, Pizzato TM, Souza FB, Mattiello-Sverzut AC (2014) Postural alignment in children with Duchenne muscular dystrophy and its relationship with balance. Braz J Phys Ther 18(2):119–126. https://doi.org/10.1590/S1413-35552012005000152

    Article  PubMed  PubMed Central  Google Scholar 

  35. Siegel IM (1972) Pathomechanics of stance in Duchenne muscular dystrophy. Arch Phys Med Rehabil 53:403–406

    CAS  PubMed  Google Scholar 

  36. Sivaraman Nair KP, Vasanth A, Gourie-Devi M, Taly AB, Rao S, Gayathri N, Murali T (2001) Disabilities in children with Duchenne muscular dystrophy: a profile. J Rehabil Med 33(4):147–149. https://doi.org/10.1080/165019701750300591

    Article  Google Scholar 

  37. Bakker JPJ, De Groot IJM, Beelen A, Lankhorst GJ (2002) Predictive factors of cessation of ambulation in patients with Duchenne muscular dystrophy. Am J Phys Med Rehabil 81:906–912. https://doi.org/10.1097/00002060-200212000-00004

    Article  PubMed  Google Scholar 

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Acknowledgements

We acknowledge all the participants with Duchenne muscular dystrophy and healthy volunteers included in the study.

Author information

Authors and Affiliations

  1. Faculty of Physical Therapy and Rehabilitation, Hacettepe University, Talatpaşa Bulvarı, 06100, Altındağ/Ankara, Turkey

    Merve Bora, Ali Yalçin, Numan Bulut, Öznur Yilmaz, Semra Topuz & İpek Alemdaroğlu-Gürbüz

  2. Department of Physiotherapy and Rehabilitation, Faculty of Health Sciences, Lokman Hekim University, Sogutozu, 06510, Çankaya/Ankara, Turkey

    Ayşe Karaduman

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Contributions

All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Merve Bora, Öznur Yilmaz, Ayşe Karaduman, Semra Topuz, İpek Alemdaroğlu-Gürbüz, Numan Bulut, and Ali Yalçin. The first draft of the manuscript was written by Merve Bora and İpek Alemdaroğlu-Gürbüz, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to İpek Alemdaroğlu-Gürbüz.

Ethics declarations

Ethics approval

This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the ethics committee of Hacettepe University (Date: 03.04.19/No.: GO 19/323).

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Informed consent to participate was obtained by children and their parents included in the study.

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Informed consent to publish was obtained by children and their parents included in the study.

Conflict of interest

The authors declare no competing interests.

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This article is a part of a comprehensive MSc thesis, named “The Evaluation of Muscle Activation During Stair Climbing Activity in Children with Duchenne Muscular Dystrophy.”

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Bora, M., Yalçin, A., Bulut, N. et al. Investigation of surface electromyography amplitude values during stair climbing task in children with Duchenne muscular dystrophy. Neurol Sci 43, 2791–2801 (2022). https://doi.org/10.1007/s10072-021-05643-y

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