Introduction

Cervical spinal cord injury is a common cause of chronic ventilatory failure and the degree of diaphragm paralysis is an important determinant of long-term respiratory support. We found only one study, which had measured the magnitude and direction of cephalocaudal diaphragm movement in subjects with diaphragm paralysis.1 Ultrasound is a well tolerated and reliable instrument for measuring diaphragm movement.2 The aim of our study was to use ultrasound to measure diaphragm movement in a group of subjects with C1–C5 cervical spinal cord injury.

Materials and methods

Subject recruitment was undertaken by the Medical Director at Hampstead Rehabilitation Centre in Adelaide. Subjects were included if they were over 18 years of age, had a spinal cord injury between C1 and C5 with an American Spinal Injury Association (ASIA) A, B or C classification and could spontaneously ventilate for 10 min. Subjects were excluded if they had any other past medical history, which could have affected their diaphragm function.

A Siemens Sonoline Antares ultrasound system (Siemens Sonoline Antares, Issaquah, WA, USA) was used to measure diaphragm movement. This system is reported to be accurate to within 0.5 mm on the basis of measurements against a phantom distance marker. Patients were positioned as upright as possible in their wheelchair or in bed. The 3.5-MHz abdominal probe was placed below the right subcostal margin between the mid-axillary and mid-clavicular line following the method described by the earlier authors.2, 3, 4

After five tidal breaths the sonographer froze the screen at the end of passive expiration and the leading edge of the diaphragm was marked on the screen using a single electronic marker. This was considered to be the position of the diaphragm at functional residual capacity. The position of the diaphragm at the end of inspiration was then marked electronically and the distance between markers was measured using inbuilt electronic calipers. The direction of the diaphragm movement from functional residual capacity was recorded for each breath. Three measurements were taken for tidal inspiration and three for maximal inspiration. Data were tabulated for descriptive analysis. The reliability of this test protocol was established (r2=0.85) using ten healthy subjects in a test retest study, which found no significant difference between average measures of diaphragm movement across the two testing days (P=0.457) or within the two test days (P=0.834) (Table 2).

We certify that all applicable institution and governmental regulations concerning the ethical use of human volunteers were followed during the course of this research.

Results

Three male subjects were tested (Table 1). Subjects 1 and 3 had reduced diaphragm movement for tidal breaths (Table 1) compared with values for normal subjects (Table 2). The magnitude of movement for maximal breaths was also reduced in these two subjects compared with earlier reported values for healthy adults in the upright sitting position (53±16 mm4).

Table 1 Descriptive and interval data for the three subjects
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Table 2 Raw data of diaphragm movement (+ mm) from the reliability study of 10 healthy subjects in upright sitting
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Discussion

The diaphragm moved in a caudal direction during all inspiratory breaths except during a maximal inspiratory breath in Subject 3.

Subject 1 (ASIA A C4/5)

The caudal direction of movement may have been because of residual innervation of the diaphragm. The small magnitude of movement may have been because of the partial paralysis of the diaphragm along with the relative recency of injury and therefore more compliant rib cage.

Subject 2 (ASIA C C3/4)

This subject had an incomplete spinal cord injury; therefore, the diaphragm was likely to be receiving innervation from the phrenic nucleus. The high magnitude of caudal movement suggests that the diaphragm was compensating for the dennervation of other respiratory muscles, whereas the chronicity of injury, with a stiffer rib cage, may have increased the piston effect of the diaphragm.

Subject 3 (ASIA A C2/3)

Subject 3 could only to be positioned at a 20-degree incline in bed on the day of testing. This position may have caused some lengthening of the diaphragm assisting diaphragm action.5 There was caudal displacement of the diaphragm during tidal breaths, which may have been because of some residual innervation and there was paradoxical (cephalad) diaphragm movement during maximal breaths. This was considered to be because of the generation of sufficient negative intra-thoracic pressure by the remaining accessory muscles during maximal breaths to overcome the minimally active diaphragm. The small magnitude of the cephalad movement was likely to be because of the chronically altered length of the diaphragm.

Conclusion

In this study of three tetraplegic subjects, imaging of diaphragm movement using B-mode ultrasound was well tolerated and able to measure both direction and magnitude of diaphragm movement during tidal and maximal inspiratory breaths. The difference in magnitude of diaphragm movement was not fully explained by the level of injury and ASIA classification and may have been because of some residual innervation of the diaphragm, time since injury, or subject position.