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Medicine & Science in Sports & Exercise:
doi: 10.1249/MSS.0b013e31822b7441
Applied Sciences

Resting Cardiopulmonary Function in Paralympic Athletes with Cervical Spinal Cord Injury

WEST, CHRISTOPHER R.1; CAMPBELL, IAN G.1; SHAVE, ROBERT E.1,2; ROMER, LEE M.1

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Author Information

1Centre for Sports Medicine and Human Performance, Brunel University, Middlesex, UNITED KINGDOM; and 2Cardiff School of Sport, University of Wales Institute, Cardiff, UNITED KINGDOM

Address for correspondence: Lee Mark Romer, Ph.D., Centre for Sports Medicine and Human Performance, Brunel University, Middlesex UB8 3PH, United Kingdom; E-mail: lee.romer@brunel.ac.uk.

Submitted for publication April 2011.

Accepted for publication June 2011.

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Abstract

Purpose: The purposes of this study were to describe resting cardiopulmonary function in highly trained athletes with cervical spinal cord injury (SCI) and to compare the data with able-bodied (AB) control subjects.

Methods: Twelve Paralympic wheelchair rugby players with cervical SCI (injury level = C5–C7) and 12 AB controls matched for age, stature, and body mass were assessed for pulmonary function using spirometry, body plethysmography, and maximal inspiratory and expiratory mouth pressures; diaphragm function using magnetic stimulation of the phrenic nerves; and cardiac function using transthoracic echocardiography.

Results: Total lung capacity, vital capacity, inspiratory reserve volume, and expiratory reserve volume were lower in SCI compared with AB (P < 0.01), whereas residual volume was elevated in SCI (P = 0.022). Airway resistance and maximal inspiratory mouth pressure were not different between groups (P > 0.41), whereas maximal expiratory mouth pressure, maximal transdiaphragmatic pressure, and twitch transdiaphragmatic pressure were lower in SCI (P < 0.01). Percent predicted total lung capacity was significantly correlated with maximal transdiaphragmatic pressure in SCI (r = 0.74), suggesting that the pulmonary restriction was a result of diaphragm weakness. Left ventricular mass, ejection fraction, stroke volume, and cardiac output were lower in SCI (P < 0.04), but early and late filling velocities during diastole were not different between groups (P > 0.05).

Conclusions: Highly trained athletes with cervical SCI exhibit a restrictive pulmonary defect, weakness of the expiratory and diaphragm muscles, atrophy of the heart, and reduced systolic cardiac function.

Individuals with cervical spinal cord injury (SCI) exhibit pulmonary restriction (2), pulmonary obstruction (30), and ventilatory muscle weakness (24). Inspiratory function is relatively well preserved in those with low cervical SCI (C5–C7), but a reduction in chest wall compliance and an increase in abdominal compliance impair the ability of the diaphragm to generate pressure (34,38). Expiratory function is also impaired because of denervation of the abdominal muscles (24).

There is some evidence that pulmonary function may be improved with short-term exercise training in individuals with SCI (32). Two studies have reported small but significant increases in vital capacity (VC) (33,36). However, the interventions were relatively short (6 wk), and individuals with cervical SCI were not studied. In the only study to have assessed pulmonary function in athletes with cervical SCI who exercised chronically (40), VC and forced expiratory volume in 1 s (FEV1) were higher than typically reported for untrained individuals with cervical SCI. It is unknown whether chronic exercise training elicits adaptations in other aspects of ventilatory function in this population.

Abolition of the venous muscle pump and loss of supraspinal sympathetic control in individuals with cervical SCI may increase venous blood pooling in the lower limbs and abdominal viscera (21). The consequent decrease in venous return, in combination with a reduced circulating blood volume (18), contributes to the lower left ventricular dimensions and mass as well as the lower stroke volume (SV) and cardiac output (Q˙) that have been reported for untrained individuals with cervical SCI compared with able-bodied (AB) individuals (7,20).

Only one study has assessed cardiac structure and function in response to exercise training in individuals with cervical SCI (27). That study found a reversal of myocardial atrophy, whereby left ventricular mass (LVM) increased by 35% after 6 months of electrically stimulated cycling exercise (27). In the AB population, chronic exercise training is associated with morphological changes in the heart, including increases in left ventricular chamber size, wall thickness, and mass (35). It is unknown whether chronic upper body exercise training provides sufficient stress to counteract the cardiac atrophy in individuals with cervical SCI.

Wheelchair rugby is the only high-intensity sport designed specifically for individuals with cervical SCI. As such, Paralympic wheelchair rugby players are an ideal population in whom to assess the chronic effects of exercise training on cardiopulmonary function in cervical SCI. Furthermore, an understanding of cardiopulmonary function in wheelchair rugby players is of interest to those involved in disability sport and those who use exercise as a tool during rehabilitation. Thus, the aims of this study were to describe resting cardiopulmonary function in a group of highly trained Paralympic wheelchair rugby players and to compare the data with an AB control group.

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METHODS

Participants

Twelve Paralympic athletes with traumatic cervical SCI (10 males) and 12 recreationally active AB individuals (10 males) matched for age (mean ± SD = 30.0 ± 5.2 vs 28.2 ± 5.7 yr), stature (1.75 ± 0.13 vs 1.73 ± 0.07 m), and body mass (66.5 ± 15.1 vs 71.3 ± 9.2 kg) volunteered to participate in the study. The participants with SCI were members of the Great Britain wheelchair rugby squad and were 9.4 ± 4.0 yr after injury. They had ≥3 yr of competitive wheelchair rugby experience and were undertaking ≥15 h·wk−1 of endurance and resistance training at the time of the study. The participants with SCI were classified using the International Standards for Neurological Classification of Spinal Cord Injury (3) and the International Wheelchair Rugby Federation classification system (10). Of the 12 participants with SCI, 11 had complete tetraplegia (C5–C7, American Spinal Injury Association (ASIA) A), and one had sensory incomplete tetraplegia (C5–C6, ASIA B). The following International Wheelchair Rugby Federation functional classifications were represented: 0.5 (n = 1), 1 (n = 3), 1.5 (n = 2), 2 (n = 2), and 2.5 (n = 4). None of the participants smoked or had a history of acute or chronic cardiopulmonary disease. The study was approved by the Brunel University Research Ethics Committee, and all participants provided written informed consent.

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Pretest Preparation

Participants were instructed to arrive at the laboratory in a rested and fully hydrated state, at least 2 h after a meal, and to avoid strenuous exercise in the 24 h before testing. The participants were also asked to refrain from caffeine and alcohol for 12 and 24 h before testing, respectively. On arrival at the laboratory, the participants with SCI were asked to void their bladder to minimize the risk of autonomic dysreflexia (21). Participants with SCI self-reported stature and completed a medical questionnaire relating to their injury.

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Experimental Procedures
Pulmonary function

Pulmonary volumes, capacities, and flows were assessed using spirometry and body plethysmography (ZAN 530; nSpire Health, Hertford, UK). Before assessment, the pneumotachograph was calibrated for volume and the plethysmograph was calibrated for pressure according to the manufacturer’s guidelines. Participants sat in a chair with arm and back supports and were instructed to maintain a stable head position throughout all maneuvers (1). First, airway resistance (Raw) during regular tidal breathing was measured between flow rates of ±0.5 L·s−1 (23). Next, functional residual capacity (FRC), slow and forced VC, FEV1, peak expiratory flow (PEF), peak inspiratory flow (PIF), and maximal voluntary ventilation in 12 s (MVV12) were assessed according to American Thoracic Society/European Respiratory Society guidelines (25,39) and adapted for SCI (19). Total lung capacity (TLC), inspiratory capacity (IC), and residual volume (RV) were derived from the pulmonary function measurements.

Maximal inspiratory pressure (PImax) and maximal expiratory pressure (PEmax) were assessed using a handheld pressure meter (MicroRPM; Micro Medical, Ltd., Kent, UK) with a flanged mouthpiece. PImax and PEmax were measured from FRC and TLC, respectively. To minimize the recruitment of buccal muscles during the PEmax maneuver and to prevent glottic closure during the inspiratory maneuver, a small 2-mm leak was incorporated into the pressure meter. An experimenter supported the participant’s cheeks during the PEmax maneuver to further minimize the use of the buccal muscles. A minimum of three and a maximum of eight maneuvers were performed at 30-s intervals, and the maximum of three measurements that varied by <10% was recorded (14).

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Inspiratory muscle function

Gastric pressure (Pga) and esophageal pressure (Pes) were measured using two latex balloon-tipped catheters (no. 47-9005; Ackrad Labs, Cooper Surgical, Berlin, Germany). Both catheters were passed pernasally into the stomach and filled with 1 mL of air. The esophageal catheter was withdrawn until a negative pressure deflection was observed during inspiration and then withdrawn an additional 10 cm to ensure that it was completely in the esophagus. Placement of the balloons was confirmed using the occlusion technique (4). Each catheter was connected to a differential pressure transducer (DP45; Validyne, Northridge, CA; range = ±229 cm H2O) that was calibrated across the physiological range using a digital pressure meter (model C9553; JMW, Ltd., Harlow, UK). The pressure signals were amplified (CD280; Validyne), digitized at a sampling rate of 150 Hz with an analog-to-digital converter (Micro1401 mkII; Cambridge Electronic Design, Cambridge, United Kingdom), and acquired using computer software (Spike2 version 7.04; Cambridge Electronic Design). Transdiaphragmatic pressure (Pdi) was obtained by online subtraction of Pes from Pga.

Magnetic stimuli were delivered to the phrenic nerve roots using two 45-mm figure-of-eight coils, each of which was powered by a monopulse magnetic stimulator (Magstim 200; Magstim, Whitland, United Kingdom). A digital output from the analog-to-digital converter was used to discharge both stimulators simultaneously. The magnetic coils were placed on either side of the neck at the posterior border of the sternocleidomastoid muscle at the level of the cricoid cartilage (26). Stimulations were performed at the end of a tidal expiration against an occluded airway. All twitches were performed from FRC at 100% of each stimulator’s power output. Three stimulations, each separated by 30 s, were delivered to the phrenic nerves. Amplitude (peak − baseline) of the diaphragm pressure response was analyzed for each of the stimulations, and the mean was recorded.

Pdi swings and ventilatory indices were assessed during 2 min of tidal breathing. The diaphragm pressure–time index (PTIdi) was calculated as the product of the tidal Pdi swing/

Equation (Uncited)
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and the inspiratory duty cycle (TI/TTOT) (5), where

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Equation (Uncited)
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is the Pdi (baseline to peak) recorded during a maximal Müeller maneuver. Minute ventilation, tidal volume, respiratory frequency, and inspiratory time (TI) were assessed using an ultrasonic flow meter (Birmingham Flowmetrics Ltd., Birmingham, United Kingdom).

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Cardiovascular function

Two-dimensional echocardiography was performed by one of the investigators (CW). Participants transferred to an echocardiography table and rested in the left lateral decubitus position for 5 min. Images were recorded with a 1.5- to 4-MHz phased-array transducer on a commercially available ultrasound system (Vivid 7; GE Medical, Horton, Norway). Left ventricular end-systolic volume (ESV), end-diastolic volume (EDV), ejection fraction (EF), and SV were determined from the apical four-chamber view using the modified single-plane Simpson method. HR was recorded simultaneously to echocardiographic images using a three-lead ECG. Q˙ was calculated as the product of HR and SV. Transmitral filling velocities during early (E) and late (A) diastole were assessed using pulsed-wave Doppler at the mitral leaflet tips. Myocardial tissue velocities during systole (S′), early diastole (E′), and late diastole (A′) were assessed using pulsed-wave tissue Doppler imaging of the septal wall at the level of the mitral annulus. Five consecutive cardiac cycles were recorded at the end of a tidal expiration, and the mean value was recorded for each parameter. LVM was calculated according to Devereux et al. (9).

Systolic blood pressure (SBP) and diastolic blood pressure (DBP) were calculated from an arterial pressure wave measured continuously with a finger cuff (Finometer PRO; Finapress Medical Systems BV, Smart Medical, Amsterdam, The Netherlands) during 5 min of rest in the seated position. The arterial wave form was sampled at 100 Hz (Micro1401 mkII; Cambridge Electronic Design) and acquired using computer software (Spike2 version 7; Cambridge Electronic Design). Mean arterial pressure (MAP) was calculated as DBP plus one-third pulse pressure (SBP − DBP).

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Statistics

Group mean differences for participant characteristics and absolute values for cardiopulmonary function were analyzed using independent-samples t-tests. Associations between continuous outcome variables were assessed using the Pearson product–moment correlation. Statistical significance was set at P < 0.05. Data are reported as means ± SD. Statistical analyses were performed using SPSS 16.0 for Windows (Chicago, IL).

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RESULTS

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Pulmonary function

Group mean values for pulmonary function are shown in Table 1. Values for TLC, IC, and VC were lower in SCI compared with AB (P < 0.01; Fig. 1). Expiratory reserve volume was lower (P = 0.003), whereas RV was higher (P = 0.022) in SCI; hence, there was no difference in FRC (P = 0.55). Furthermore, FEV1, PEF, PIF, and MVV12 were lower in SCI (P < 0.013). There were no differences in Raw between groups. PImax was not different between groups (P = 0.41), but PEmax was lower in SCI (P = 0.004).

Table 1
Table 1
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Figure 1
Figure 1
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Inspiratory muscle function

Group mean values for inspiratory muscle function are shown in Table 2.

Table 2
Table 2
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and

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were lower in SCI compared with AB (P < 0.001) primarily because of a lower Pga contribution (P < 0.001). Tidal pressure swings were not different between groups (P > 0.46). Consequently, Pdi/

Equation (Uncited)
Equation (Uncited)
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during resting breathing was elevated in SCI (P < 0.015). Neither PTIdi nor ventilatory indices were different between groups (P > 0.34). In SCI, percent predicted TLC correlated with

Equation (Uncited)
Equation (Uncited)
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(r = 0.74, P = 0.036) but not with PImax (r = 0.12, P = 0.78).

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Cardiovascular function

Group mean values for cardiovascular function are shown in Table 3. Participants with SCI demonstrated lower LVM (P = 0.030), left ventricular internal diameter during systole (P = 0.003) and diastole (P = 0.030), and EDV (P = 0.004). Consequently, Q˙ (P = 0.004), SV (P = 0.006), and EF (P = 0.028) were lower in SCI. SBP (P < 0.001), DBP (P = 0.017), MAP (P = 0.001) were also lower in SCI.

Table 3
Table 3
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DISCUSSION

This is the first study to comprehensively describe resting cardiopulmonary function in athletes with cervical SCI. Compared with AB controls, Paralympic athletes with cervical SCI exhibited pulmonary restriction but not obstruction, as evidenced by the lower TLC and similar Raw, respectively. Global inspiratory muscle strength (i.e., PImax) was similar between groups, but expiratory muscle strength (i.e., PEmax) and diaphragm muscle function (i.e.,

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and

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) were reduced in SCI. There was also evidence of cardiac atrophy and reduced systolic function in SCI, as demonstrated by the lower LVM and EF, respectively.

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Pulmonary function

In line with previous findings in untrained individuals with cervical SCI (e.g., Anke et al. [2]), we found that TLC and VC were lower than normal in our athletes with cervical SCI. The percent predicted VC, however, was higher than typically reported for untrained individuals with cervical SCI (22). The higher VC in our athletes was likely due to superior expiratory muscle function, as demonstrated by the elevated PEmax and PEF. We attribute the enhanced expiratory muscle function to a training-induced increase in strength of the accessory muscles of expiration (11). Although our data suggest that pulmonary function improves with training, longitudinal data are needed to confirm this hypothesis.

To our knowledge, we are the first to demonstrate normal levels of airway resistance (Raw) in individuals with cervical SCI. Studies in untrained individuals with cervical SCI have documented elevated levels of Raw and have attributed this finding to loss of sympathetic control to airway smooth muscle (30). That Raw was normal in our athletes with cervical SCI suggests that the hyperpnea of chronic exercise training may have a protective effect on airway smooth muscle. In this regard, even small amounts of airway stretch have been shown to disturb the bronchiolar latch state and promote relaxation of the airway smooth muscle (13).

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Inspiratory muscle function

The pressure-generating capacity of the diaphragm in response to a maximal Müeller maneuver (

Equation (Uncited)
Equation (Uncited)
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) and magnetic stimulation of the phrenic nerves (

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) was lower in highly trained athletes with cervical SCI compared with AB controls, but similar to values reported for untrained individuals with cervical SCI (17,34). The reduced pressure-generating capacity of the diaphragm in cervical SCI seems to be due to elevated abdominal compliance, as evidenced by the significantly lower gastric contribution to Pdi. In contrast, the Pdi swing during tidal breathing was not different between groups. Accordingly, Pdi/

Equation (Uncited)
Equation (Uncited)
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was higher in cervical SCI, implying that the relative force output of the diaphragm is elevated in this population. Nevertheless, there did not seem to be any functional consequences because the PTIdi for the diaphragm did not exceed the “critical” threshold level for fatigue (5), and none of the participants reported dyspnea at rest. The similarity in diaphragm function between our highly trained athletes with cervical SCI and previously reported values for untrained individuals with cervical SCI (17,34) suggests that chronic exercise training does not improve the force-generating capacity of the diaphragm. Rather, an elevated abdominal compliance is likely the overriding factor in determining the force-generating capacity of the diaphragm in this population.

In the participants with SCI, most of the variance in TLC was accounted for by

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Equation (Uncited)
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(∼55%) rather than PImax (<2%). Thus, the pulmonary restriction observed in SCI was primarily due to weakness of the diaphragm rather than to weakness of the additional muscles of inspiration that contribute to PImax, such as the scalenes, sternocleidomastoids, and other neck muscles. In contrast, AB individuals progressively activate the scalenes and sternocleidomastoids as lung volume increases to TLC (31). The difference in response can be explained by the action of the neck muscles on the thoracic cavity. In AB, the neck muscles displace the upper rib cage cranially, thereby causing an increase in anteroposterior diameter (8). In cervical SCI, a stiff rib cage causes a decrease in tidal excursion of the upper rib cage during inspiration and, in some instances, a paradoxical inward motion of the upper rib cage. Consequently, the increase in size of the thoracic cavity during a maximal inspiration to TLC in cervical SCI is primarily due to expansion of the lower rib cage resulting from the appositional and insertional forces of the diaphragm acting through the zone of apposition (38).

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Cardiovascular function

This is the first study to assess cardiac structure and function in athletes with cervical SCI. Cardiac dimensions and LVM were smaller in athletes with SCI compared with AB controls but similar to values reported in untrained individuals with cervical SCI (7,20). The similar LVM between trained and untrained individuals with SCI suggests that the metabolic demand of the exercise training undertaken by our participants was insufficient to attenuate the degree of cardiac atrophy that is known to occur in this population (20). In this regard, we recently reported a peak oxygen uptake of only 1.20 L·min−1 for highly trained athletes with cervical SCI (37). The cardiac atrophy noted in the present study was most likely due to venous pooling below the injury (21) and a reduction in circulating blood volume (18).

In addition to the aforementioned differences in cardiac dimensions and mass, we found that EDV, Q˙, SV, and EF were also lower in SCI compared with AB. There were, however, no differences in ESV or S′ between groups; this suggests that the lower SV was explained by the lower EDV. The reason for the lower EDV in SCI is likely due to a reduction in cardiac preload, resulting from impaired sympathetic vasoconstrictor function below the lesion (21) and reduced circulating blood volume (18). In agreement with findings from studies in untrained individuals with cervical SCI (7,12), we found no difference in diastolic function between SCI and AB. The normal diastolic function in SCI may be explained by a reduction in left atrial size (i.e., cardiac atrophy), which, in the face of a reduced venous return, may result in similar left atrial pressures for SCI compared with AB. Although we have no measure of left atrial pressure, mitral inflow and E′ were similar in SCI versus AB. That a strong positive relationship exists between diastolic dysfunction and risk of heart failure (16) suggests that the cardiac atrophy noted in the present study may be a morphological adaptation that serves to maintain normal diastolic function.

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CONCLUSIONS

Compared with AB controls, highly trained athletes with cervical SCI demonstrated a restrictive pulmonary defect, weakness of the expiratory and diaphragm muscles, atrophy of the heart, and reduced systolic cardiac function. These findings suggest that chronic exercise training does not “normalize” cardiopulmonary function in cervical SCI. However, the superior pulmonary function in highly trained compared with untrained individuals with cervical SCI suggests that chronic exercise training has the potential to improve pulmonary function in this population.

The study was funded by UK Sport. The authors report no conflicts of interest.

The results of the present study do not constitute endorsement by the American College of Sports Medicine.

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REFERENCES

1. Amodie-Storey C, Nash MS, Roussell PM, Knox AW, Crane LD. Head position and its effect on pulmonary function in tetraplegic patients. Spinal Cord. 1996; 34: 602–7.

2. Anke A, Aksnes AK, Stanghelle JK, Hjeltnes N. Lung volumes in tetraplegic patients according to cervical spinal cord injury level. Scand J Rehabil Med. 1993; 25: 73–7.

3. ASIA. Reference Manual of the International Standards for Neurological Classification of Spinal Cord Injury. Chicago (IL): American Spinal Injuries Association; 2003. p. 24.

4. Baydur A, Behrakis PK, Zin WA, Jaeger M, Milic-Emili J. A simple method for assessing the validity of the esophageal balloon technique. Am Rev Respir Dis. 1982; 126: 788–91.

5. Bellemare F, Grassino A. Effect of pressure and timing of contraction on human diaphragm fatigue. J Appl Physiol. 1982; 53: 1190–5.

6. Bruschi C, Cerveri I, Zoia MC, et al.. Reference values of maximal respiratory mouth pressures: a population-based study. Am Rev Respir Dis. 1992; 146: 790–3.

7. de Groot PC, van Dijk A, Dijk E, Hopman MT. Preserved cardiac function after chronic spinal cord injury. Arch Phys Med Rehabil. 2006; 87: 1195–200.

8. De Troyer A, Estenne M. Coordination between rib cage muscles and diaphragm during quiet breathing in humans. J Appl Physiol. 1984; 57: 899–906.

9. Devereux RB, Alonso DR, Lutas EM, et al.. Echocardiographic assessment of left ventricular hypertrophy: comparison to necropsy findings. Am J Cardiol. 1986; 57: 450–8.

10. Duffield D, Hart A. International Wheelchair Rugby Federation Classification Manual. 3rd ed. Richmond, BC, Canada, International Wheelchair Rugby Federation; 2008. p. 1–25.

11. Estenne M, Knoop C, Vanvaerenbergh J, Heilporn A, De Troyer A. The effect of pectoralis muscle training in tetraplegic subjects. Am Rev Respir Dis. 1989; 139: 1218–22.

12. Eysmann SB, Douglas PS, Katz SE, Sarkarati M, Wei JY. Left ventricular mass and diastolic filling patterns in quadriplegia and implications for effects of normal aging on the heart. Am J Cardiol. 1995; 75: 201–3.

13. Fredberg JJ, Inouye D, Miller B, et al.. Airway smooth muscle, tidal stretches, and dynamically determined contractile states. Am J Respir Crit Care Med. 1997; 156: 1752–9.

14. Green M, Road J, Sieck GC, Similowski T. Tests of respiratory muscle strength. ATS/ERS Statement on respiratory muscle testing. Am J Respir Crit Care Med. 2002; 166: 518–624.

15. Grimby G, Sóderholm B. Spirometric studies in normal subjects. Acta Med Scand. 1963; 173: 199–206.

16. Grossman W. Diastolic dysfunction and congestive heart failure. Circulation. 1990; 81: III1–7.

17. Hart N, Laffont I, de la Sota AP, et al.. Respiratory effects of combined truncal and abdominal support in patients with spinal cord injury. Arch Phys Med Rehabil. 2005; 86: 1447–51.

18. Houtman S, Oeseburg B, Hopman MT. Blood volume and hemoglobin after spinal cord injury. Am J Phys Med Rehabil. 2000; 79: 260–5.

19. Kelley A, Garshick E, Gross ER, Lieberman SL, Tun CG, Brown R. Spirometry testing standards in spinal cord injury. Chest. 2003; 123: 725–30.

20. Kessler KM, Pina I, Green B, et al.. Cardiovascular findings in quadriplegic and paraplegic patients and in normal subjects. Am J Cardiol. 1986; 58: 525–30.

21. Krassioukov A. Autonomic function following cervical spinal cord injury. Respir Physiol Neurobiol. 2009; 169: 157–64.

22. Linn WS, Spungen AM, Gong H, Adkins RH, Bauman WA, Waters RL. Forced vital capacity in two large outpatient populations with chronic spinal cord injury. Spinal Cord. 2001; 39: 263–8.

23. Lord PW, Edwards JM. Variation in airways resistance when defined over different ranges of airflows. Thorax. 1978; 33: 401–5.

24. Mateus SR, Beraldo PS, Horan TA. Maximal static mouth respiratory pressure in spinal cord injured patients: correlation with motor level. Spinal Cord. 2007; 45: 569–75.

25. Miller MR, Hankinson J, Brusasco V, et al.. Standardisation of spirometry. Eur Respir J. 2005; 26: 319–38.

26. Mills GH, Kyroussis D, Hamnegard CH, Polkey MI, Green M, Moxham J. Bilateral magnetic stimulation of the phrenic nerves from an anterolateral approach. Am J Respir Crit Care Med. 1996; 154: 1099–105.

27. Nash MS, Bilsker S, Marcillo AE, et al.. Reversal of adaptive left ventricular atrophy following electrically-stimulated exercise training in human tetraplegics. Paraplegia. 1991; 29: 590–9.

28. Quanjer P. Standardized lung function testing. Bull Eur Physiopathol Respir. 1983; 19: 33–8.

29. Quanjer PH, Tammeling GJ, Cotes JE, Pedersen OF, Peslin R, Yernault JC. Lung volumes and forced ventilatory flows. Report Working Party Standardization of Lung Function Tests, European Community for Steel and Coal. Official Statement of the European Respiratory Society. Eur Respir J Suppl. 1993; 16: 5–40.

30. Radulovic M, Schilero GJ, Wecht JM, et al.. Airflow obstruction and reversibility in spinal cord injury: evidence for functional sympathetic innervation. Arch Phys Med Rehabil. 2008; 89: 2349–53.

31. Raper AJ, Thompson WT, Shapiro W, Patterson JL. Scalene and sternomastoid muscle function. J Appl Physiol. 1966; 21: 497–502.

32. Sheel AW, Reid WD, Townson AF, Ayas NT, Konnyu KJ. Effects of exercise training and inspiratory muscle training in spinal cord injury: a systematic review. J Spinal Cord Med. 2008; 31: 500–8.

33. Silva AC, Neder JA, Chiurciu MV, et al.. Effect of aerobic training on ventilatory muscle endurance of spinal cord injured men. Spinal Cord. 1998; 36: 240–5.

34. Sinderby C, Weinberg J, Sullivan L, Borg J, Lindstrom L, Grassino A. Diaphragm function in patients with cervical cord injury or prior poliomyelitis infection. Spinal Cord. 1996; 34: 204–13.

35. Spirito P, Pelliccia A, Proschan MA, et al.. Morphology of the “athlete’s heart” assessed by echocardiography in 947 elite athletes representing 27 sports. Am J Cardiol. 1994; 74: 802–6.

36. Sutbeyaz ST, Koseoglu BF, Gokkaya NK. The combined effects of controlled breathing techniques and ventilatory and upper extremity muscle exercise on cardiopulmonary responses in patients with spinal cord injury. Int J Rehabil Res. 2005; 28: 273–6.

37. Taylor BJ, West CR, Romer LM. No effect of arm-crank exercise on diaphragmatic fatigue or ventilatory constraint in Paralympic athletes with cervical spinal cord injury. J Appl Physiol. 2010; 109: 358–66.

38. Urmey W, Loring S, Mead J, et al.. Upper and lower rib cage deformation during breathing in quadriplegics. J Appl Physiol. 1986; 60: 618–22.

39. Wanger J, Clausen JL, Coates A, et al.. Standardisation of the measurement of lung volumes. Eur Respir J. 2005; 26: 511–22.

40. Wicks JR, Oldridge NB, Cameron BJ, Jones NL. Arm cranking and wheelchair ergometry in elite spinal cord–injured athletes. Med Sci Sports Exerc. 1983; 15 (3): 224–31.

Keywords:

CARDIAC; DIAPHRAGM; PHRENIC NERVE; PULMONARY; TETRAPLEGIA; ULTRASONOGRAPHY

©2012The American College of Sports Medicine

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