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Semin Respir Crit Care Med 2009; 30(3): 330-338
DOI: 10.1055/s-0029-1222447
© Thieme Medical Publishers

Hypoventilation after Spinal Cord Injury

Richard J. Castriotta1 , Jayasimha N. Murthy1
  • 1Division of Pulmonary, Critical Care, and Sleep Medicine, The University of Texas Health Science Center at Houston Medical School, Houston, Texas
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Publication History

Publication Date:
18 May 2009 (online)

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ABSTRACT

There are ~12,000 new cases per year in the United States of spinal cord injury (SCI) with life expectancies from 11 to 14 years (ventilator dependent) to 44 years (non–ventilator dependent). Those with SCI (C2–C8) are at great risk for developing hypoventilation, especially during sleep, and this risk increases along with the risk of sleep disordered breathing as they age. Most will have significantly reduced vital capacity and ventilatory reserve because of interruption of neural pathways to the diaphragm, chest, and abdomen, resulting in a restrictive ventilatory impairment with intact diffusing capacity. Diagnosis entails measurement of pCO2 with capnography both awake and during sleep, optimally along with polysomnography to evaluate for all forms of sleep disordered breathing. Treatment options include diaphragmatic pacing, full positive pressure ventilation through tracheostomy, and noninvasive positive pressure ventilation. Some may require mechanical ventilation only during sleep.

KEYWORDS

Spinal cord injury - hypoventilation - diaphragmatic paralysis - diaphragmatic pacing - sleep disordered breathing

REFERENCES

  • 1 National Spinal Cord Injury Statistical Center .Spinal Cord Injury: Facts and Figures at a Glance. Birmingham; University of Alabama at Birmingham, National Spinal Cord Injury Statistical Center; 2008 Available at http://images.main.uab.edu/spinalcord/pdffiles/Facts08.pdf Accessed November 10, 2008
    Google Scholar
  • 2 Winslow C, Rozovsky J. Effect of spinal cord injury on the respiratory system.  Am J Phys Med Rehabil. 2003;  82 803-814
    CrossrefPubMedGoogle Scholar
  • 3 National Spinal Cord Injury Statistical Center .The 2006 Annual Statistical Report for the Model Spinal Cord injury Care System. Birmingham; University of Alabama at Birmingham, National Spinal Cord Injury Statistical Center; 2006 Available at http://images.main.uab.edu/spinalcord/pdffiles/NSCIC%20Annual%2006.pdf Accessed November 10, 2008
    Google Scholar
  • 4 Zimmer M B, Nantwi K, Goshgarian H G. Effect of spinal cord injury on the respiratory system: basic research and current clinical treatment options.  J Spinal Cord Med. 2007;  30 319-330
    PubMedGoogle Scholar
  • 5 McMichan J C, Michel L, Westbrook P R. Pulmonary dysfunction following traumatic quadriplegia recognition, prevention, and treatment.  JAMA. 1980;  243 528-531
    CrossrefPubMedGoogle Scholar
  • 6 Axen K, Pineda H, Shunfenthal I, Haas F. Diaphragmatic function following cervical cord injury: neurally mediated improvement.  Arch Phys Med Rehabil. 1985;  66 219-222
    CrossrefPubMedGoogle Scholar
  • 7 De Troyer A, Estenne M. Coordination between rib cage muscles and diaphragm during quiet breathing in humans.  J Appl Physiol. 1984;  57 899-906
    PubMedGoogle Scholar
  • 8 Estenne M, De Troyer A. Relationship between respiratory muscle electromyogram and rib cage motion in tetraplegia.  Am Rev Respir Dis. 1985;  132 53-59
    PubMedGoogle Scholar
  • 9 Bergofsky E H. Relative contributions of the rib cage and the diaphragm to ventilation in man.  J Appl Physiol. 1964;  19 698-706
    PubMedGoogle Scholar
  • 10 Agostoni E, Mognoni P, Torri G, Agostoni A R. Static features of the passive rib cage and abdomen-diaphragm.  J Appl Physiol. 1965;  20 1187-1193
    PubMedGoogle Scholar
  • 11 Loring S H, Mead J. Action of the diaphragm on the rib cage inferred from a force-balance analysis.  J Appl Physiol. 1982;  53 756-760
    PubMedGoogle Scholar
  • 12 Mead J, Loring S H. Analysis of volume displacement and length changes of the diaphragm during breathing.  J Appl Physiol. 1982;  53 750-755
    PubMedGoogle Scholar
  • 13 Rochester D F. The diaphragm: contractile properties and fatigue.  J Clin Invest. 1985;  75 1397-1402
    PubMedGoogle Scholar
  • 14 Zimmer M B, Nantwi K, Goshgarian H G. Effect of spinal cord injury on the neural regulation of respiratory function.  Exp Neurol. 2008;  209 399-406
    CrossrefPubMedGoogle Scholar
  • 15 Linn W S, Adkins R H, Gong Jr H J, Waters R L. Pulmonary function in chronic spinal cord injury: a cross-sectional survey of 222 southern California adult outpatients.  Arch Phys Med Rehabil. 2000;  81 757-763
    PubMedGoogle Scholar
  • 16 Bergofsky E H. Mechanism for respiratory insufficiency after cervical cord injury; a source of alveolar hypoventilation.  Ann Intern Med. 1964;  61 435-447
    PubMedGoogle Scholar
  • 17 Estenne M, De Troyer A. The effects of tetraplegia on chest wall statics.  Am Rev Respir Dis. 1986;  134 121-124
    PubMedGoogle Scholar
  • 18 Gross D, Grassino A, Ross W R, Macklem P T. Electromyogram pattern of diaphragmatic fatigue.  J Appl Physiol. 1979;  46 1-7
    PubMedGoogle Scholar
  • 19 Gross D, Grassino A, Scott G, Ladd H, Macklem P T. Respiratory muscle fatigue in quadriplegic patients.  Clin Res. 1977;  25 713A
    PubMedGoogle Scholar
  • 20 Feldman J L, Del Negro C A. Looking for inspiration: new perspectives on respiratory rhythm.  Nat Rev Neurosci. 2006;  7 232-242
    CrossrefPubMedGoogle Scholar
  • 21 Onimaru H, Homma I. A novel functional neuron group for respiratory rhythm generation in the ventral medulla.  J Neurosci. 2003;  23 1478-1486
    PubMedGoogle Scholar
  • 22 Smith J C, Ellenberger H H, Ballanyi K, Richter D W, Feldman J L. Pre-Bötzinger complex: a brainstem region that may generate respiratory rhythm in mammals.  Science. 1991;  254 726-729
    CrossrefPubMedGoogle Scholar
  • 23 Hollinshead W H, Keswani N H. Localization of the phrenic nucleus in the spinal cord of man.  Anat Rec. 1956;  125 683-699
    PubMedGoogle Scholar
  • 24 Routal R V, Pal G P. Location of the phrenic nucleus in the human spinal cord.  J Anat. 1999;  195(Pt 4) 617-621
    CrossrefPubMedGoogle Scholar
  • 25 McKay L C, Feldman J L. Unilateral ablation of pre-Botzinger complex disrupts breathing during sleep but not wakefulness.  Am J Respir Crit Care Med. 2008;  178 89-95
    CrossrefPubMedGoogle Scholar
  • 26 Bulow K. Respiration in wakefulness in man.  Acta Physiol Scand Suppl. 1963;  209 1-110
    PubMedGoogle Scholar
  • 27 Douglas N J, White D P, Pickett C K, Weil J V, Zwillich C W. Respiration during sleep in normal man.  Thorax. 1982;  37 840-844
    CrossrefPubMedGoogle Scholar
  • 28 Douglas N J, White D P, Weil J V, Pickett C K, Zwillich C W. Hypercapnic ventilatory response in sleeping adults.  Am Rev Respir Dis. 1982;  126 758-762
    PubMedGoogle Scholar
  • 29 Douglas N J, White D P, Weil J V et al.. Hypoxic ventilatory response decreases during sleep in normal men.  Am Rev Respir Dis. 1982;  125 286-289
    PubMedGoogle Scholar
  • 30 Haas F, Axen K, Pineda H, Gandino D, Haas A. Temporal pulmonary function changes in cervical cord injury.  Arch Phys Med Rehabil. 1985;  66 139-144
    PubMedGoogle Scholar
  • 31 Bach J R, Wang T G. Pulmonary function and sleep disordered breathing in patients with traumatic tetraplegia: a longitudinal study.  Arch Phys Med Rehabil. 1994;  75 279-284
    CrossrefPubMedGoogle Scholar
  • 32 Linn W S, Spungen A M, Gong Jr H J, Adkins R H, Bauman W A, Waters R L. Forced vital capacity in two large outpatient populations with chronic spinal cord injury.  Spinal Cord. 2001;  39 263-268
    CrossrefPubMedGoogle Scholar
  • 33 McEvoy R D, Mykytyn I, Sajkov D et al.. Sleep apnoea in patients with quadriplegia.  Thorax. 1995;  50 613-619
    PubMedGoogle Scholar
  • 34 Burns S P, Kapur V, Yin K S, Buhrer R. Factors associated with sleep apnea in men with spinal cord injury: a population-based case-control study.  Spinal Cord. 2001;  39 15-22
    CrossrefPubMedGoogle Scholar
  • 35 Stockhammer E, Tobon A, Michel F et al.. Characteristics of sleep apnea syndrome in tetraplegic patients.  Spinal Cord. 2002;  40 286-294
    CrossrefPubMedGoogle Scholar
  • 36 Flavell H, Marshall R, Thornton A T, Clements P L, Antic R, McEvoy R D. Hypoxia episodes during sleep in high tetraplegia.  Arch Phys Med Rehabil. 1992;  73 623-627
    PubMedGoogle Scholar
  • 37 Lu K, Lee T C, Liang C L, Chen H J. Delayed apnea in patients with mid- to lower cervical spinal cord injury.  Spine. 2000;  25 1332-1338
    CrossrefPubMedGoogle Scholar
  • 38 Bach J R, Intintola P, Alba A S, Holland I E. The ventilator-assisted individual: cost analysis of institutionalization vs rehabilitation and in-home management.  Chest. 1992;  101 26-30
    CrossrefPubMedGoogle Scholar
  • 39 Bach J R. Alternative methods of ventilatory support for the patient with ventilatory failure due to spinal cord injury.  J Am Paraplegia Soc. 1991;  14 158-174
    PubMedGoogle Scholar
  • 40 Bach J R, Alba A S. Management of chronic alveolar hypoventilation by nasal ventilation.  Chest. 1990;  97 52-57
    PubMedGoogle Scholar
  • 41 Bach J R. New approaches in the rehabilitation of the traumatic high level quadriplegic.  Am J Phys Med Rehabil. 1991;  70 13-19
    PubMedGoogle Scholar
  • 42 Bach J R. A comparison of long-term ventilatory support alternatives from the perspective of the patient and care giver.  Chest. 1993;  104 1702-1706
    PubMedGoogle Scholar
  • 43 Bach J R, Saporito L R. Criteria for extubation and tracheostomy tube removal for patients with ventilatory failure: a different approach to weaning.  Chest. 1996;  110 1566-1571
    CrossrefPubMedGoogle Scholar
  • 44 Steier J, Jolley C J, Seymour J et al.. Sleep-disordered breathing in unilateral diaphragm paralysis or severe weakness.  Eur Respir J. 2008;  32 1479-1487
    CrossrefPubMedGoogle Scholar
  • 45 Guilleminault C, Philip P, Robinson A. Sleep and neuromuscular disease: bilevel positive airway pressure by nasal mask as a treatment for sleep disordered breathing in patients with neuromuscular disease.  J Neurol Neurosurg Psychiatry. 1998;  65 225-232
    PubMedGoogle Scholar
  • 46 Ayas N T, Brown R, Shea S A. Hypercapnia can induce arousal from sleep in the absence of altered respiratory mechanoreception.  Am J Respir Crit Care Med. 2000;  162(3 Pt 1) 1004-1008
    PubMedGoogle Scholar
  • 47 Ferguson G T, Gilmartin M. CO2 rebreathing during BiPAP ventilatory assistance.  Am J Respir Crit Care Med. 1995;  151 1126-1135
    PubMedGoogle Scholar
  • 48 Bach J R. Continuous noninvasive ventilation for patients with neuromuscular disease and spinal cord injury.  Semin Respir Crit Care Med. 2002;  23 283-292
    Article in Thieme ConnectPubMedGoogle Scholar
  • 49 Allam J S, Olson E J, Gay P C, Morgenthaler T I. Efficacy of adaptive servoventilation in treatment of complex and central sleep apnea syndromes.  Chest. 2007;  132 1839-1846
    CrossrefPubMedGoogle Scholar
  • 50 Morgenthaler T I, Gay P C, Gordon N, Brown L K. Adaptive servoventilation versus noninvasive positive pressure ventilation for central, mixed, and complex sleep apnea syndromes.  Sleep. 2007;  30 468-475
    PubMedGoogle Scholar
  • 51 Javaheri S, Malik A, Smith J, Chung E. Adaptive pressure support servoventilation: a novel treatment for sleep apnea associated with use of opioids.  J Clin Sleep Med. 2008;  4 305-310
    PubMedGoogle Scholar
  • 52 Farney R J, Walker J M, Boyle K M, Cloward T V, Shilling K C. Adaptive servoventilation (ASV) in patients with sleep disordered breathing associated with chronic opioid medications for non-malignant pain.  J Clin Sleep Med. 2008;  4 311-319
    PubMedGoogle Scholar
  • 53 Ambrogio C, Lowman X, Kuo M, Malo J, Prasad A R, Parthasarathy S. Sleep and non-invasive ventilation in patients with chronic respiratory insufficiency.  Intensive Care Med. 2009;  35 306-313
    CrossrefPubMedGoogle Scholar
  • 54 Storre J H, Seuthe B, Fiechter R et al.. Average volume-assured pressure support in obesity hypoventilation: a randomized crossover trial.  Chest. 2006;  130 815-821
    CrossrefPubMedGoogle Scholar
  • 55 Glenn W W, Hogan J F, Phelps M L. Ventilatory support of the quadriplegic patient with respiratory paralysis by diaphragm pacing.  Surg Clin North Am. 1980;  60 1055-1078
    PubMedGoogle Scholar
  • 56 Glenn W W, Hogan J F, Loke J S, Ciesielski T E, Phelps M L, Rowedder R. Ventilatory support by pacing of the conditioned diaphragm in quadriplegia.  N Engl J Med. 1984;  310 1150-1155
    PubMedGoogle Scholar
  • 57 Glenn W W, Phelps M L. Diaphragm pacing by electrical stimulation of the phrenic nerve.  Neurosurgery. 1985;  17 974-984
    CrossrefPubMedGoogle Scholar
  • 58 Shaul D B, Danielson P D, McComb J G, Keens T G. Thoracoscopic placement of phrenic nerve electrodes for diaphragmatic pacing in children.  J Pediatr Surg. 2002;  37 974-978, discussion 974–978
    CrossrefPubMedGoogle Scholar
  • 59 Elefteriades J A, Quin J A, Hogan J F et al.. Long-term follow-up of pacing of the conditioned diaphragm in quadriplegia.  Pacing Clin Electrophysiol. 2002;  25 897-906
    CrossrefPubMedGoogle Scholar
  • 60 Alshekhlee A, Onders R P, Syed T U, Elmo M, Katirji B. Phrenic nerve conduction studies in spinal cord injury: applications for diaphragmatic pacing.  Muscle Nerve. 2008;  38 1546-1552
    CrossrefPubMedGoogle Scholar
  • 61 Glenn W W, Sairenji H. Diaphragm pacing in the treatment of chronic ventilatory insufficiency. In: Roussos C, Macklem P The Thorax: Lung Biology in Health and Disease. New York; Marcel Dekker 1985: 1407-1440
    Google Scholar
  • 62 Shaw R K, Glenn W W, Hogan J F, Phelps M L. Electrophysiological evaluation of phrenic nerve function in candidates for diaphragm pacing.  J Neurosurg. 1980;  53 345-354
    PubMedGoogle Scholar
  • 63 Mier A, Brophy C, Moxham J, Green M. Twitch pressures in the assessment of diaphragm weakness.  Thorax. 1989;  44 990-996
    PubMedGoogle Scholar
  • 64 Esclarín A, Bravo P, Arroyo O, Mazaira J, Garrido H, Alcaraz M A. Tracheostomy ventilation versus diaphragmatic pacemaker ventilation in high spinal cord injury.  Paraplegia. 1994;  32 687-693
    PubMedGoogle Scholar
  • 65 Hirschfeld S, Exner G, Luukkaala T, Baer G A. Mechanical ventilation or phrenic nerve stimulation for treatment of spinal cord injury-induced respiratory insufficiency.  Spinal Cord. 2008;  46 738-742
    CrossrefPubMedGoogle Scholar
  • 66 DiMarco A F, Onders R P, Ignagni A, Kowalski K E, Mortimer J T. Phrenic nerve pacing via intramuscular diaphragm electrodes in tetraplegic subjects.  Chest. 2005;  127 671-678
    CrossrefPubMedGoogle Scholar
  • 67 DiMarco A F, Connors Jr A FJ, Kowalski K E. Gas exchange during separate diaphragm and intercostal muscle breathing.  J Appl Physiol. 2004;  96 2120-2124
    CrossrefPubMedGoogle Scholar
  • 68 Van Houtte S, Vanlandewijck Y, Gosselink R. Respiratory muscle training in persons with spinal cord injury: a systematic review.  Respir Med. 2006;  100 1886-1895
    CrossrefPubMedGoogle Scholar
  • 69 Van Houtte S, Vanlandewijck Y, Kiekens C, Spengler C M, Gosselink R. Patients with acute spinal cord injury benefit from normocapnic hyperpnoea training.  J Rehabil Med. 2008;  40 119-125
    CrossrefPubMedGoogle Scholar
  • 70 Urmey W, Loring S, Mead J et al.. Upper and lower rib cage deformation during breathing in quadriplegics.  J Appl Physiol. 1986;  60 618-622
    PubMedGoogle Scholar
  • 71 McCool F D, Pichurko B M, Slutsky A S, Sarkarati M, Rossier A, Brown R. Changes in lung volume and rib cage configuration with abdominal binding in quadriplegia.  J Appl Physiol. 1986;  60 1198-1202
    PubMedGoogle Scholar
  • 72 Kajana S, Goshgarian H G. Administration of phosphodiesterase inhibitors and an adenosine A1 receptor antagonist induces phrenic nerve recovery in high cervical spinal cord injured rats.  Exp Neurol. 2008;  210 671-680
    CrossrefPubMedGoogle Scholar
  • 73 Tzelepis G E, Bascom A T, Safwan Badr M, Goshgarian H G. Effects of theophylline on pulmonary function in patients with traumatic tetraplegia.  J Spinal Cord Med. 2006;  29 227-233
    PubMedGoogle Scholar

Richard J CastriottaM.D. 

Division of Pulmonary, Critical Care, and Sleep Medicine, The University of Texas Health Science Center at Houston Medical School

6431 Fannin St., MSB 1.274, Houston, TX 72019

Email: Richard.J.Castriotta@uth.tmc.edu

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