Journal of Neurology

, Volume 260, Issue 5, pp 1295–1303 | Cite as

Oral muscles are progressively affected in Duchenne muscular dystrophy: implications for dysphagia treatment

  • Lenie van den Engel-Hoek
  • Corrie E. Erasmus
  • Jan C. M. Hendriks
  • Alexander C. H. Geurts
  • Willemijn M. Klein
  • Sigrid Pillen
  • Lilian T. Sie
  • Bert J. M. de Swart
  • Imelda J. M. de Groot
Original Communication


Dysphagia is reported in advanced stages of Duchenne muscular dystrophy (DMD). The population of DMD is changing due to an increasing survival. We aimed to describe the dysphagia in consecutive stages and to assess the underlying mechanisms of dysphagia in DMD, in order to develop mechanism based recommendations for safe swallowing. In this cross-sectional study, participants were divided into: early and late ambulatory stage (AS, n = 6), early non-ambulatory stage (ENAS, n = 7), and late non-ambulatory stage (LNAS, n = 11). Quantitative oral muscle ultrasound was performed to quantify echo intensity. Swallowing was assessed with a video fluoroscopic swallow study, surface electromyography (sEMG) of the submental muscle group and tongue pressure. Differences in outcome parameters among the three DMD stages were tested with analysis of variance. Oral muscles related to swallowing were progressively affected, starting in the AS with the geniohyoid muscle. Tongue (pseudo) hypertrophy was found in 70 % of patients in the ENAS and LNAS. Oral phase problems and post-swallow residue were observed, mostly in the LNAS with solid food. sEMG and tongue pressure data of swallowing solid food revealed the lowest sEMG amplitude, the longest duration and lowest tongue pressure in the LNAS. In case of swallowing problems in DMD, based on the disturbed mechanisms of swallowing, it is suggested to (1) adjust meals in terms of less solid food, and (2) drink water after meals to clear the oropharyngeal area.


Duchenne muscular dystrophy Dysphagia Oral muscles Ultrasound Video fluoroscopic swallow study Surface electromyography 



This work was funded by the Duchenne Parent Project (The Netherlands). The authors wish to thank the patients and their parents for participating in the study. The authors also wish to thank Karen van Hulst, MSc (Radboud University Medical Centre, Nijmegen, The Netherlands, Department of Rehabilitation) for analyzing the VFSS.

Conflicts of interest

The authors declare that they have no conflict of interest.


  1. 1.
    Reimers K, Reimers CD, Wagner S, Paetzke I, Pongratz DE (1993) Skeletal muscle sonography: a correlative study of echogenicity and morphology. J Ultrasound Med 12:73–77PubMedGoogle Scholar
  2. 2.
    Bushby K, Finkel R, Birnkrant DJ et al (2010) Diagnosis and management of Duchenne muscular dystrophy, part 1: diagnosis, and pharmacological and psychosocial management. Lancet Neurol 9:77–93PubMedCrossRefGoogle Scholar
  3. 3.
    Shinonaga C, Fukuda M, Suzuki Y et al (2008) Evaluation of swallowing function in Duchenne muscular dystrophy. Dev Med Child Neurol 50:478–480PubMedCrossRefGoogle Scholar
  4. 4.
    Hanayama K, Liu M, Higuchi Y et al (2008) Dysphagia in patients with Duchenne muscular dystrophy evaluated with a questionnaire and videofluorography. Disabil Rehabil 30:517–522PubMedCrossRefGoogle Scholar
  5. 5.
    Aloysius A, Born P, Kinali M, Davis T, Pane M, Mercuri E (2008) Swallowing difficulties in Duchenne muscular dystrophy: indications for feeding assessment and outcome of videofluroscopic swallow studies. Eur J Paediatr Neurol 12:239–245PubMedCrossRefGoogle Scholar
  6. 6.
    Pane M, Vasta I, Messina S et al (2006) Feeding problems and weight gain in Duchenne muscular dystrophy. Eur J Paediatr Neurol 10:231–236PubMedCrossRefGoogle Scholar
  7. 7.
    Ono T, Hori K, Tamine K, Maeda Y (2009) Evaluation of tongue motor biomechanics during swallowing—from oral feeding models to quantitative sensing methods. Jpn Dent Sci Rev 45:65–74CrossRefGoogle Scholar
  8. 8.
    Steele CM, van Lieshout P (2009) Tongue movements during water swallowing in healthy young and older adults. J Speech Lang Hear Res 52:1255–1267PubMedCrossRefGoogle Scholar
  9. 9.
    Yeates EM, Steele CM, Pelletier CA (2010) Tongue pressure and submental surface electromyography measures during non effortful and effortful saliva swallows in healthy women. Am J Speech Lang Pathol 19:274–281PubMedCrossRefGoogle Scholar
  10. 10.
    Vaiman M, Segal S, Eviatar E (2004) Surface electromyographic studies of swallowing in normal children, age 4–12 years. Int J Pediatr Otorhinolaryngol 68:65–73PubMedCrossRefGoogle Scholar
  11. 11.
    Scholten RR, Pillen S, Verrips A, Zwarts MJ (2003) Quantitative ultrasonography of skeletal muscles in children: normal values. Muscle Nerve 27:693–698PubMedCrossRefGoogle Scholar
  12. 12.
    Pillen S, Tak RO, Zwarts MJ et al (2009) Skeletal muscle ultrasound: correlation between fibrous tissue and echo intensity. Ultrasound Med Biol 35:443–446PubMedCrossRefGoogle Scholar
  13. 13.
    van den Engel-Hoek L, van Alfen N, de Swart BJM, de Groot IJM, Pillen S (2012) Quantitative ultrasound of the tongue and submental muscles in children and young adults. Muscle Nerve 46:31–37CrossRefGoogle Scholar
  14. 14.
    van der Wilt GJ, Zielhuis GA (2008) Merging evidence-based and mechanism-based medicine. Lancet 372:519–520PubMedCrossRefGoogle Scholar
  15. 15.
    Berard C, Payan C, Hodgkinson I, Fermanian J (2005) A motor function measure for neuromuscular diseases. Construction and validation study. Neuromuscul Disord 15:463–470PubMedCrossRefGoogle Scholar
  16. 16.
    van den Engel-Hoek L, Erasmus CE, van Bruggen HW et al (2009) Dysphagia in spinal muscular atrophy type II: more than a bulbar problem? Neurology 73:1787–1791PubMedCrossRefGoogle Scholar
  17. 17.
    Arvedson JC (2008) Assessment of pediatric dysphagia and feeding disorders: clinical and instrumental approaches. Dev Disabil Res Rev 14:118–127PubMedCrossRefGoogle Scholar
  18. 18.
    van den Engel-Hoek L, de Groot IJM, Esser E et al (2012) Biomechanical events of swallowing are determined more by bolus consistency than by age or gender. Physiol Behav 106:285–290PubMedCrossRefGoogle Scholar
  19. 19.
    Steele CM, Bailey GL, Molfenter SM (2010) Tongue pressure modulation during swallowing: water versus nectar-thick liquids. J Speech Lang Hear Res 53:273–283PubMedCrossRefGoogle Scholar
  20. 20.
    Palmer PM, Jaffe DM, McCulloch TM, Finnegan EM, Van Daele DJ, Luschei ES (2008) Quantitative contributions of the muscles of the tongue, floor-of-mouth, jaw, and velum to tongue-to-palate pressure generation. J Speech Lang Hear Res 51:828–835PubMedCrossRefGoogle Scholar
  21. 21.
    Jansen M, van Alfen N, van der Nijhuis Sanden M, van Dijk J, Pillen S, de Groot IJM (2012) Quantitative muscle ultrasound is a promising longitudinal follow-up tool in Duchenne muscular dystrophy. Neuromuscul Disord 22:306–317PubMedCrossRefGoogle Scholar
  22. 22.
    Kim Y, McCullough GH, Asp CW (2005) Temporal measurements of pharyngeal swallowing in normal populations. Dysphagia 20:290–296PubMedCrossRefGoogle Scholar
  23. 23.
    Steele CM, Bailey GL, Chau T et al (2011) The relationship between hyoid and laryngeal displacement and swallowing impairment. Clin Otolaryngol 36:30–36PubMedCrossRefGoogle Scholar
  24. 24.
    Weir K, McMahon S, Barry L, Ware R, Masters IB, Chang AB (2007) Oropharyngeal aspiration and pneumonia in children. Pediatr Pulmonol 42:1024–1331PubMedCrossRefGoogle Scholar
  25. 25.
    Spassov A, Gredes T, Gedrange T, Lucke S, Pavlovic D, Kunert-Keil C (2010) Histological changes in masticatory muscles of mdx mice. Arch Oral Biol 55:318–324PubMedCrossRefGoogle Scholar
  26. 26.
    Kent RD (2004) The uniqueness of speech among motor systems. Clin Linguist Phon 18:495–505PubMedCrossRefGoogle Scholar
  27. 27.
    Jansen M, de Groot IJM, van Alfen N, Geurts AC (2010) Physical training in boys with Duchenne muscular dystrophy: the protocol of the no use is disuse study. BMC Pediatr 10:55PubMedGoogle Scholar
  28. 28.
    Youmans SR, Stierwalt JA (2006) Measures of tongue function related to normal swallowing. Dysphagia 21:102–111PubMedCrossRefGoogle Scholar
  29. 29.
    Torriani M, Townsend E, Thomas BJ, Bredella MA, Ghomi RH, Tseng BS (2012) Lower leg muscle involvement in Duchenne muscular dystrophy: an MR imaging and spectroscopy study. Skeletal Radiol 41:437–445PubMedCrossRefGoogle Scholar
  30. 30.
    Beenakker EA, de Vries J, Fock JM et al (2002) Quantitative assessment of calf circumference in Duchenne muscular dystrophy patients. Neuromuscul Disord 12:639–642PubMedCrossRefGoogle Scholar
  31. 31.
    Marden FA, Connolly AM, Siegel MJ, Rubin DA (2005) Compositional analysis of muscle in boys with Duchenne muscular dystrophy using MR imaging. Skeletal Radiol 34:140–148PubMedCrossRefGoogle Scholar
  32. 32.
    Ramdharry GM (2010) Rehabilitation in practice: management of lower motor neuron weakness. Clin Rehabil 24:387–397PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Lenie van den Engel-Hoek
    • 1
  • Corrie E. Erasmus
    • 2
  • Jan C. M. Hendriks
    • 3
  • Alexander C. H. Geurts
    • 1
  • Willemijn M. Klein
    • 4
  • Sigrid Pillen
    • 2
  • Lilian T. Sie
    • 2
  • Bert J. M. de Swart
    • 1
  • Imelda J. M. de Groot
    • 1
  1. 1.Department of Rehabilitation, Nijmegen Centre for Evidence Based PracticeRadboud University Medical Centre, NijmegenNijmegenThe Netherlands
  2. 2.Department of Pediatric NeurologyRadboud University Medical Centre, NijmegenNijmegenThe Netherlands
  3. 3.Department of Epidemiology, Biostatistics and HTARadboud University Medical Centre, NijmegenNijmegenThe Netherlands
  4. 4.Department of RadiologyRadboud University Medical Centre, NijmegenNijmegenThe Netherlands

Personalised recommendations