Original article| Volume 93, ISSUE 11, P1950-1956, November 2012

Pulmonary Function and Expiratory Flow Limitation in Acute Cervical Spinal Cord Injury

Published:April 30, 2012DOI:


      Alvisi V, Marangoni E, Zannoli S, Uneddu M, Uggento R, Farabegoli L, Ragazzi R, Milic-Emili J, Belloni GP, Alvisi R, Volta CA. Pulmonary function and expiratory flow limitation in acute cervical spinal cord injury.


      To identify the nature of the changes of respiratory mechanics in patients with middle cervical spinal cord injury (SCI) and their correlation with posture.


      Clinical trial.


      Acute SCI unit.


      Patients with SCI (N=34) at C4-5 level studied within 6 months of injury.


      Patients were assessed by the negative expiratory pressure test, maximal static respiratory pressure test, and standard spirometry.

      Main Outcome Measures

      The following respiratory variables were recorded in both the semirecumbent and supine positions: (1) tidal expiratory flow limitation (TEFL); (2) airway resistances; (3) mouth occlusion pressure developed 0.1 seconds after occluded inspiration at functional residual capacity (P0.1); (4) maximal static inspiratory pressure (MIP) and maximal static expiratory pressure (MEP); and (5) spirometric data.


      TEFL was detected in 32% of the patients in the supine position and in 9% in the semirecumbent position. Airway resistances and P0.1 were much higher compared with normative values, while MIP and MEP were markedly reduced. The ratio of forced expiratory volume in 1 second to forced vital capacity was less than 70%, while the other spirometric data were reduced up to 30% of predicted values.


      Patients with middle cervical SCI can develop TEFL. The presence of TEFL, associated with increased airway resistance, could increase the work of breathing in the presence of a reduced capacity of the respiratory muscles to respond to the increased load. The semirecumbent position and the use of continuous positive airway pressure can be helpful to (1) reduce the extent of TEFL and avoid the opening/closure of the small airways; (2) decrease airway resistance; and (3) maintain the expiratory flow as high as possible, which aids in the removal of secretions.

      Key Words

      List of Abbreviations:

      ATS (American Thoracic Society), ERV (expiratory reserve volume), FEV1 (forced expiratory volume in 1 second), FRC (functional residual capacity), FVC (forced vital capacity), IC (inspiratory capacity), MEP (maximal static expiratory pressure), MIP (maximal static inspiratory pressure), NEP (negative expiratory pressure), P0.1 (mouth occlusion pressure developed 0.1 seconds after occluded inspiration at functional residual capacity), PEEPe (extrinsic positive end-expiratory pressure), RV (residual volume), SCI (spinal cord injury), TEFL (tidal expiratory flow limitation), V (volume), V' (flow), VT (tidal volume), VC (vital capacity)
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        • van den Berg M.E.L.
        • Castellote J.M.
        • De Pedro-Cuesta J.
        • Mahillo-Fernandez I.
        Survival after spinal cord injury: a systematic review.
        J Neurotrauma. 2010; 27: 1517-1528
        • Winslow C.
        • Rozovsky J.
        Effect of spinal cord injury on the respiratory system.
        Am J Phys Med Rehabil. 2003; 82: 803-814
        • Linn W.S.
        • Adkins R.H.
        • Gong Jr, H.
        • 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
        • Milic-Emili J.
        • Torchio R.
        • D'Angelo E.
        Closing volume: a reappraisal (1967-2007).
        Eur J Appl Physiol. 2007; 99: 567-583
        • Pelosi P.
        • Rocco P.R.M.
        Airway closure: the silent killer of peripheral airways.
        Crit Care. 2007; 11: 114
        • Bake B.
        • Fugl-Meyer A.R.
        • Grimby G.
        Breathing patterns and regional ventilation distribution in tetraplegic patients and in normal subjects.
        Clin Sci. 1972; 42: 117-128
        • Estenne M.
        • De Troyer A.
        Mechanism of the postural dependence of vital capacity in tetraplegic subjects.
        Am Rev Respir Dis. 1987; 135: 367-371
        • Lumb A.B.
        Elastic forces and lung volume.
        in: Lumb A.B. Nunn's applied respiratory physiology. 6th ed. Butterworth-Heinemann, Philadelphia2005: 25-38
        • Koulouris N.G.
        • Valta P.
        • Lavoie A.
        • et al.
        A simple method to detect expiratory flow limitation during spontaneous breathing.
        Eur Respir J. 1995; 8: 306-313
        • Estenne M.
        • Van Muylem A.
        • Gorini M.
        • Kinnear W.
        • Heilporn A.
        • De Troyer A.
        Evidence of dynamic airway compression during cough in tetraplegic patients.
        Am J Respir Crit Care Med. 1994; 150: 1081-1085
        • Mead J.
        • Turner J.M.
        • Macklem P.T.
        • Little J.B.
        Significance of the relationship between lung recoil and maximum expiratory flow.
        J Appl Physiol. 1967; 22: 95-108
        • Lumb A.B.
        Respiratory system resistance.
        in: Lumb A.B. Nunn's applied respiratory physiology. 6th ed. Butterworth-Heinemann, Philadelphia2005: 39-54
        • Roussos C.
        • Koutsoukou A.
        Respiratory failure.
        Eur Respir J. 2003; 22: 3s-14s
        • Eltayara L.
        • Rigsby Becklake M.
        • Volta C.A.
        • Milic-Emili J.
        Relationship between chronic dyspnea and expiratory flow limitation in patients with chronic obstructive pulmonary disease.
        Am J Respir Crit Care Med. 1996; 154: 1726-1734
        • Koutsoukou A.
        • Bekos B.
        • Sotiropoulou C.
        • Koulouris N.G.
        • Roussos C.
        • Milic-Emili J.
        Effect of positive end-expiratory pressure on gas exchange and expiratory flow limitation in adult respiratory distress syndrome.
        Crit Care Med. 2002; 30: 1941-1949
        • Rossi A.
        • Polese G.
        • Milic-Emili J.
        Monitoring respiratory mechanics in ventilator-dependent patients.
        in: Tobin M.J. Principles and practice of intensive care monitoring. McGraw-Hill, New York1998: 583-584
        • Miller M.R.
        • ATS/ERS Task Force
        Standardisation of spirometry.
        Eur Respir J. 2005; 26: 319-338
        • Whitelaw W.A.
        • Derenne J.P.
        • Milic-Emili J.
        Occlusion pressure as a measure of respiratory center output in conscious man.
        Respir Physiol. 1975; 292: 1029-1030
        • American Thoracic Society/European Respiratory Society
        Statement on respiratory muscles testing.
        Am J Respir Crit Care Med. 2002; 166: 518-524
        • Quanjer P.H.
        • Tammeling G.J.
        • Cotes J.E.
        • Pedersen O.F.
        • Peslin R.
        • Yernault J.C.
        Lung volumes and forced ventilatory flows.
        Eur Respir J Suppl. 1993; 16: 5-40
        • Baydur A.
        • Adkins R.H.
        • Milic-Emili J.
        Lung mechanics in individuals with spinal cord injury: effects of injury level and posture.
        J Appl Physiol. 2001; 90: 405-411
        • D'Angelo E.
        • Pecchiari M.
        • Saetta M.
        • Balestro E.
        • Milic-Emili J.
        Dependence of lung injury on inflation rate during low-volume ventilation in normal open-chest rabbits.
        J Appl Physiol. 2004; 97: 260-268
        • Davis K.J.R.
        • Campbell R.S.
        • Johannigman J.A.
        • Valente J.F.
        • Branson R.D.
        Changes in respiratory mechanics after tracheostomy.
        Arch Surg. 1999; 134: 59-62
        • Milic-Emili J.
        Respiratory mechanics in chest wall disease: implications for expiratory flow limitation during resting breathing.
        Monaldi Arch Chest Dis. 1993; 1: 80-82
        • Hogg J.C.
        • Macklem P.T.
        • Thurlbeck W.M.
        Site and nature of airway obstruction in chronic obstructive lung disease.
        N Engl J Med. 1968; 278: 1355-1360
        • Baydur A.
        • Milic-Emili J.
        Expiratory flow limitation during spontaneous breathing: comparison of patients with restrictive and obstructive respiratory disorders.
        Chest. 1997; 112: 1017-1023
        • Kiwerski J.E.
        Factors contributing to the increased threat to life following spinal cord injury.
        Paraplegia. 1993; 31: 793-799
        • Huldtgren A.C.
        • Fugl-Meyer A.R.
        • Jonasson E.
        • Bake B.
        Ventilatory dysfunction and respiratory rehabilitation in post-traumatic quadriplegia.
        Eur Respir J. 1988; 1: 242-247
        • Mateus S.R.M.
        • Beraldo P.S.S.
        • Horan T.A.
        Maximal static mouth respiratory pressure in spinal cord injured patients: correlations with motor level.
        Spinal Cord. 2007; 45: 569-575
        • Sinderby C.
        • Weinberg J.
        • Sullivan L.
        • Borg J.
        • Lindström L.
        • Grassino A.
        Diaphragm function in patients with cervical cord injury or prior poliomyelitis infection.
        Spinal Cord. 1996; 34: 204-213
        • Mueller G.
        • de Groot S.
        • van der Woude L.
        • Hopman M.T.
        Time-courses of lung function and respiratory muscles pressure generating capacity after spinal cord injury: a prospective cohort study.
        J Rehabil Med. 2008; 40: 269-276
        • Laghi F.
        • Tobin M.J.
        Disorders of the respiratory muscles.
        Am J Respir Crit Care Med. 2003; 168: 10-48
        • Huang C.C.
        • Tsai Y.H.
        • Lin M.C.
        • Yang C.T.
        • Hsieh M.J.
        • Lan R.S.
        Respiratory drive and pulmonary mechanics during haemodialysis with ultrafiltration in ventilated patients.
        Anaesth Intensive Care. 1997; 25: 464-470
        • Lendsome J.R.
        • Sharp J.M.
        Pulmonary function in acute cervical cord injury.
        Am Rev Respir Dis. 1981; 124: 41-44
        • Knudson R.J.
        • Clark D.F.
        • Kennedy T.C.
        • Knudson D.E.
        Effect of aging alone on mechanical properties of the normal adult human lung.
        J Appl Physiol. 1977; 43: 1054-1062
        • Sulc J.
        • Volta C.A.
        • Ploysongsang Y.
        • Eltayara L.
        • Olivenstein R.
        • Milic-Emili J.
        Flow limitation and dyspnoea in normal supine subjects during methacholine challenge.
        Eur Respir J. 1999; 14: 1326-1331
        • McCarthy D.S.
        • Spencer R.
        • Creene R.
        • Milic-Emili J.
        Measurement of “closing volume” as a simple and sensitive test for early detection of small airway disease.
        Am J Med. 1972; 52: 747-753
        • Burrows B.
        • Knudson R.J.
        • Cline M.G.
        • Lebowitz M.D.
        Quantitative relationships between cigarette smoking and ventilatory function.
        Am Rev Respir Dis. 1977; 115: 195-205
        • The Acute Respiratory Distress Syndrome Network
        Ventilation with lower tidal volumes as compared with traditional tidal volumes for acute lung injury and the acute respiratory distress syndrome.
        N Engl J Med. 2000; 342: 1301-1308
        • Bergofsky E.H.
        Mechanism for respiratory insufficiency after cervical cord injury.
        Ann Intern Med. 1964; 61: 435-447
        • Harvey L.A.
        • Ellis E.R.
        The effect of continuous positive airway pressures on lung volumes in tetraplegic patients.
        Paraplegia. 1996; 34: 54-58