Archives of Physical Medicine and Rehabilitation
Volume 90, Issue 5 , Pages 717-725 , May 2009

Lower Thoracic Spinal Cord Stimulation to Restore Cough in Patients With Spinal Cord Injury: Results of a National Institutes of Health–Sponsored Clinical Trial. Part I: Methodology and Effectiveness of Expiratory Muscle Activation

Presented in part to the Congress of Neurological Surgeons, October 7–12, 2006, Chicago, IL; the American Spinal Injury Association, May 30–June 2, 2007, Tampa, FL; the International Spinal Cord Society, June 27–July 1, 2007, Reykjavik, Iceland; the American Paraplegia Society, August 27–29, 2007, Orlando, FL; the American Academy of Physical Medicine and Rehabilitation, September 27–30, 2007, Boston, MA; the American Thoracic Society, May 16–21, 2008, Toronto, ON, Canada; and the American Spinal Injury Association, August 8–11, 2008, Orlando, FL.

  • Anthony F. DiMarco, MD

      Affiliations

    • Department of Physiology and Biophysics, Case Western Reserve University, Cleveland, OH
    • Corresponding Author InformationCorrespondence to Anthony F. DiMarco, MD, MetroHealth Medical Center, Rammelkamp Center for Education and Research, 2500 MetroHealth Dr, Cleveland, OH 44109
    • ,
  • Krzysztof E. Kowalski, PhD

      Affiliations

    • Department of Physiology and Biophysics, Case Western Reserve University, Cleveland, OH
    • ,
  • Robert T. Geertman, MD, PhD

      Affiliations

    • Department of Neurological Surgery, Case Western Reserve University, Cleveland, OH
    • Division of Neurological Surgery, MetroHealth Medical Center, Cleveland, OH
    • ,
  • Dana R. Hromyak, BS

      Affiliations

    • Department of Physiology and Biophysics, Case Western Reserve University, Cleveland, OH

References 

  1. DeTroyer A, Estenne M, Heilporn A. Mechanism of active expiration in tetraplegic subjects. N Engl J Med. 1986;314:740–744
  2. Estenne M, DeTroyer A. Cough in tetraplegic subjects: an active process. Ann Intern Med. 1990;112:22–28
  3. Kelly BJ. Luce JM (The diagnosis and management of neuromuscular diseases causing respiratory failure). Chest. 1991;99:1485–1494
  4. McMichan JC, Michel L, Westbrook PR. Pulmonary dysfunction following traumatic quadriplegia: recognition, prevention and treatment. JAMA. 1980;243:528–531
  5. Carter RE. Respiratory aspects of spinal cord injury management. Paraplegia. 1987;25:262–266
  6. Jackson AB, Groomes TE. Incidence of respiratory complications following spinal cord injury. Arch Phys Med Rehabil. 1994;75:270–275
  7. Brown R, DiMarco AF, Hoit JD, Garshick E. Respiratory dysfunction and management in spinal cord injury. Respir Care. 2006;51:853–870
  8. Zimmer MB, Nantwi K, Goshgarian HG. Effect of spinal cord injury on the respiratory system: basic research and current clinical treatment options. J Spinal Cord Med. 2007;30:319–330
  9. Homnick DN. Mechanical insufflation-exsufflation for airway mucus clearance. Respir Care. 2007;52:1296–1307
  10. Sivasothy P, Brown L, Smith IE, Shneerson JM. Effect of manually assisted cough and mechanical insufflation on cough flow of normal subjects, patients with chronic obstructive pulmonary disease (COPD), and patients with respiratory muscle weakness. Thorax. 2001;56:438–444
  11. Chatwin M, Ross E, Hart N, Nickol AH, Polkey MI, Simonds AK. Cough augmentation with mechanical insufflation/exsufflation in patients with neuromuscular weakness. Eur Respir J. 2003;21:502–508
  12. Bach JR. Mechanical insufflation-exsufflation: comparison of peak expiratory flows with manually assisted and unassisted coughing techniques. Chest. 1993;104:1553–1562
  13. Kiwerski JE. Factors contributing to the increased threat of life following spinal cord injury. Paraplegia. 1993;31:793–799
  14. Hartkopp A, Bronnum-Hansen H, Seidenschnur AM, Biering-Sorensen F. Survival and cause of death after traumatic spinal cord injury: a long-term epidemiological survey from Denmark. Spinal Cord. 1997;35:76–85
  15. Frankel HL, Coll JR, Charlifue SW, et al. Long-term survival in spinal cord injury: a fifty year investigation. Spinal Cord. 1998;36:266–274
  16. DeVivo MJ, Krause JS, Lammertse DP. Recent trends in mortality and causes of death among persons with spinal cord injury. Arch Phys Med Rehabil. 1999;80:1411–1419
  17. Jaeger RJ, Langbein EW, Kralj AR. Augmenting cough by FES in tetraplegia: a comparison of results at three clinical centers. Basic Appl Myol. 1994;4:195–200
  18. DiMarco AF, Romaniuk JR, Supinski GS. Electrical activation of the expiratory muscles to restore cough. Am J Respir Crit Care Med. 1995;151:1466–1471
  19. Jaeger RJ, Turba RM, Yarkony GM, Roth EJ. Cough in spinal cord injured patients: comparison of three methods to produce cough. Arch Phys Med Rehabil. 1993;74:1358–1361
  20. Lin VWH, Hsieh C, Hsiao IN, Canfield J. Functional magnetic stimulation of expiratory muscles: a noninvasive and new method for restoring cough. J Appl Physiol. 1998;84:1144–1150
  21. Kyroussis D, Polkey MI, Mills GH, Hughes PD, Moxham J, Green M. Stimulation of cough in man by magnetic stimulation of the thoracic nerve roots. Am J Respir Crit Care Med. 1997;156:1696–1699
  22. DiMarco AF, Romaniuk JR, Kowalski KE, Supinski G. Pattern of expiratory muscle activation during lower thoracic spinal cord stimulation. J Appl Physiol. 1999;86:1881–1889
  23. DiMarco AF, Kowalski KE, Supinski G, Romaniuk JR. Mechanism of expiratory muscle activation during lower thoracic spinal cord stimulation. J Appl Physiol. 2002;92:2341–2346
  24. DiMarco AF, Kowalski KE, Geertman RT, et al. Lower thoracic spinal cord stimulation to restore cough in patients with spinal cord injury: results of an NIH sponsored clinical trial (Part II: clinical outcomes). Arch Phys Med Rehabil. 2009;90:726–732
  25. DiMarco AF, Kowalski KE, Geertman RT, Hromyak DR. Spinal cord stimulation: a new method to produce an effective cough in patients with spinal cord injury. Am J Respir Crit Care Med. 2006;173:1386–1389
  26. DiMarco AF, Kowalski KE. Effects of chronic electrical stimulation on paralyzed expiratory muscles. J Appl Phisol. 2008;104:1634–1640
  27. Ferguson AS, Stone HE, Roessmann U, Burke M, Tisdale E, Mortimer JT. Muscle plasticity: comparison of a 30-Hz burst with 10-Hz continuous stimulation. J Appl Physiol. 1989;66:1143–1151
  28. Pette D, Vrbova G. What does chronic electrical stimulation teach us about muscle plasticity?. Muscle Nerve. 1999;22:666–677
  29. Loudon RG, Shaw GB. Mechanics of cough in normal subjects and in patients with obstructive respiratory disease. Am Rev Respir Dis. 1967;96:666–677
  30. Langlands J. The dynamics of cough in health and in chronic bronchitis. Thorax. 1967;22:88–96
  31. Arora NS, Gal TJ. Cough dynamics during progressive expiratory muscle weakness in healthy curarized subjects. J Appl Physiol. 1981;51:494–498
  32. Siebens AA, Kirby NA, Poulos DA. Cough following transection of spinal cord at C-6. Arch Phys Med Rehabil. 1964;45:1–8
  33. Black LF, Hyatt RE. Maximal respiratory pressures: normal values and relationship to age and sex. Am Rev Respir Dis. 1969;99:696–702
  34. Bach JR, Ishikawa Y, Kim H. Prevention of pulmonary morbidity for patients with Duchenne muscular dystrophy. Chest. 1997;112:1024–1028
  35. Woodburne RT. Essentials of human anatomy. New York: Oxford University Press; 1969;
  36. Miller ME, Chrisensen GC, Eveans E. Anatomy of the dog. Philadelphia: WB Saunders; 1964;
  37. DiMarco AF, Romaniuk JR, Kowalski KE, Supinski G. Mechanical contribution of expiratory muscles to pressure generation during spinal cord stimulation. J Appl Physiol. 1999;87:1433–1439
  38. Polkey MI, Luo Y, Guleria R, Hamnegård CH, Green M, Moxham J. Functional magnetic stimulation of the abdominal muscles in humans. Am J Respir Crit Care Med. 1999;160:513–522
  39. Lin VW, Singh H, Chitkara RK, Perkash I. Functional magnetic stimulation for restoring cough in patients with tetraplegia. Arch Phys Med Rehabil. 1998;79:517–522
  40. Linder SH. Functional electrical stimulation to enhance cough in quadriplegia. Chest. 1993;103:166–169
  41. Lim J, Gorman RB, Saboisky JP, Gandevia SC, Butler JE. Optimal electrode placement for noninvasive electrical stimulation of human abdominal muscles. J Appl Physiol. 2007;102:1612–1617
  42. Turner JA, Loeser JD, Deyo RA, Sanders SB. Spinal cord stimulation for patients with failed back surgery syndrome or complex regional pain syndrome: a systematic review of effectiveness and complications. Pain. 2004;108:137–147
  43. Taylor RS, Van Buyten JP, Buchser E. Spinal cord stimulation for complex regional pain syndrome: a systematic review of the clinical and cost-effectiveness literature and assessment of prognostic factors. Eur J Pain. 2006;10:91–101
  44. Taylor RS, Van Buyten JP, Buchser E. Spinal cord stimulation for chronic back and leg pain and failed back surgery syndrome: a systematic review and analysis of prognostic factors. Spine. 2004;30:152–160
  45. Kumar K, Buchser E, Linderoth B, Meglio M, Van Buyten JP. Avoiding complications from spinal cord stimulation: practical recommendations from an international panel of experts. Neuromodulation. 2007;10:24–33

 Supported by the National Institute of Neurological Disorders and Stroke (grant no. R01 NS049516) and the National Center for Research Resources (grant no. M01 RR 00080 and UL1 RR024989). Clinical Trial Registration Number: NCT00116337.

 We certify that we have affiliations with or financial involvement (eg, employment, consultancies, honoraria, stock ownership or options, expert testimony, grants and patents received or pending, royalties) with an organization or entity with a financial interest in, or financial conflict with, the subject matter or materials discussed in the article. Dr. DiMarco is a founder of and has a significant financial interest in Synapse BioMedical, Inc, a manufacturer of diaphragm pacing systems.

 Reprints are not available from the author.

PII: S0003-9993(09)00123-3

doi: 10.1016/j.apmr.2008.11.013

Archives of Physical Medicine and Rehabilitation
Volume 90, Issue 5 , Pages 717-725 , May 2009

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