1Respiratory Muscle Laboratory, Department of Thoracic Medicine, Royal Brompton Hospital, London, UK. 2Department of Anaesthetics, Kings College Hospital, London, UK. 3Department of Pulmonary Medicine and Clinical Physiology, Sahlgrenska University Hospital, Goteborg, Sweden. 4Respiratory Muscle Laboratory, Department of Thoracic Medicine, Kings College Hospital, London, UK*Corresponding author: Department of Surgical and Anaesthetic Sciences, K floor, Royal Hallamshire Hospital, Sheffield S10 2 JF, UK
Accepted for publication: July 31, 2001
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Abstract |
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Br J Anaesth 2001; 87: 87684
Keywords: muscle skeletal, diaphragm; equipment, tubes tracheal; intensive care
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Introduction |
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Conventionally, balloon catheters are passed into the oesophagus and stomach to measure pressure above and below the diaphragm. The difference between these two pressures is transdiaphragmatic pressure, which is an index of diaphragmatic strength during phrenic nerve stimulation.3 4 However, the requirement for balloon catheters makes these methods invasive. The oesophageal and gastric balloon are difficult to position and the measurement is subject to artefact, especially when supine and in the presence of atelectasis. A means of gauging mean pleural or oesophageal pressure change in response to diaphragmatic contraction, by measuring airway or tracheal tube pressure, would facilitate the assessment of diaphragm strength on the ICU.
Pressures measured at the mouth during phrenic nerve stimulation (twitch mouth pressure) have already been used in ambulant patients with electrical and cervical magnetic stimulation,5 6 although glottic closure can be a problem when mouth pressures are compared with twitch oesophageal pressure (TwPoes). This would not be a problem in the intubated patient, when twitch tracheal tube pressure (TwPet) is measured.
Non-volitional tests of diaphragm strength conventionally require electrical stimulation of the phrenic nerves. However, the adequacy and consistency of stimulation may be a problem because of the need to position the stimulating electrodes precisely over the nerves.7 The technique of bilateral anterolateral magnetic stimulation (BAMPS) over the surface markings of the phrenic nerves in the neck, allows supramaximal bilateral phrenic stimulation in supine patients, without the need for neck flexion, which is required with the cervical approach.8 This produces a pattern of stimulation very similar to bilateral electrical stimulation (BES).9 10
Therefore, if the BAMPS technique could be combined with TwPet measurements, this would provide a non-volitional and non-invasive assessment of diaphragm strength on the ICU. These recordings would allow us to assess more readily diaphragmatic strength in the ventilated patient and so help the complex assessment of the balance between the capacity of the respiratory system and the load placed upon it, particularly during weaning from respiratory support.
However, even though posture has little effect on TwPdi it does affect the ratio of the decrease in oesophageal pressure to the increase in gastric pressure that make up the change in transdiaphragmatic pressure.9 11 For example, when the diaphragm is stimulated to contract in the supine position there is a larger decrease in twitch oesophageal pressure (TwPoes) than when sitting, but a relatively smaller contribution from the increase in gastric pressure (TwPgas), so overall twitch transdiaphragmatic pressure (TwPdi) is little affected by posture (Fig. 1).11 Therefore, it was necessary to assess our new technique in both the supine position, when the oesophageal pressure contribution to changes in TwPdi would be high, and in the sitting poition where the gastric component, which would not be measured by twitch tracheal tube pressure (TwPet), would be greater, to determine if a useful relationship between TwPet and TwPes or TwPet and TwPdi could be established in the two postures.
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We therefore aimed to measure twitch TwPet proximal to an occluded tracheal tube, during BAMPS in the supine and sitting position, to determine whether this reliably reflected oesophageal pressure change during diaphragmatic contraction and could, therefore, act as an indicator of TwPdi in intubated patients.13
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Methods |
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Measurements
Pressure measurements were made from oesophageal and gastric balloon catheters14 (PK Morgan, Rainham, Kent, UK), passed through the nose shortly after induction of anaesthesia via a long uncuffed red rubber nasotracheal tube, which had been passed into the oesophagus and then removed once the balloons were in place. Appropriate positioning of the balloons was initially confirmed using the technique of Ducros.15 Later, once spontaneous breathing had been resumed, the position of the balloons was once more confirmed by occluding the tracheal tube and asking the patient to make a gentle inspiratory effort;16 if the balloons were correctly positioned the change in tracheal tube pressure equalled the change in Poes. Pressure measurements were also made from the proximal end of the tracheal tube via a catheter of similar material, length, and diameter as the balloon catheter tubing.
Phrenic nerve stimulation
The phrenic nerves were stimulated with two 43-mm mean diameter double coils placed anterolaterally on the neck over the phrenic nerves. Each double coil was powered by a Magstim 200HP stimulator (The Magstim Company, Whitland, Dyfed, Wales, UK). The stimulators were charged to 100% of maximum power and triggered simultaneously. This level of power output is known to produce stimulation which is supramaximal or very close to being so.9
Changes in lung volume alter the position of the inspiratory muscles and so influence apparent diaphragm strength. For example, at high lung volumes the diaphragm is flattened, so reducing its ability to generate negative intrathoracic pressures during a maximal contraction. On the other hand, reductions in lung volume increase the curvature of the diaphragm and increase its ability to generate inspiratory pressures,17 18 but are associated with atelectasis and worsened compliance.
The effect of potentiation may confuse diaphragm strength measurements. A fully potentiated twitch is 50% larger than a twitch in the same subject when fully rested.19 20 This makes exact comparisons of strength more difficult to interpret unless patients can be rested for 20 min, avoiding all vigorous respiratory efforts before testing. On the ICU this could be achieved by providing adequate respiratory support.
Study design
To minimize potentiation,19 20 all subjects were observed for 20 min to ensure that no vigorous respiratory efforts were made. Potentiation is the phenomenon whereby twitch amplitude depends on the recent contractile history of the muscle. Providing a muscle has not worked so hard that it is fatigued, a recent maximal voluntary contraction will temporarily alter the behaviour of the muscle so that it produces a twitch up to 50% greater than normal amplitude in response to a single twitch stimulation. This effect lasts for 20 min. Manipulations involving the tracheal tube were made as gently as possible to avoid stimulating the airway, which might lead to contractions that could potentiate the diaphragm. Then the tracheal tube was momentarily occluded and the phrenic nerves stimulated. Stimulations were made at end-expiration and before the next inspiration during mechanical ventilation. Those subjects who were spontaneously breathing on the tracheal tube via a T piece, were asked to breath in time with instructions and then relax at the end-expiratory position. The tracheal tube was then occluded and the phrenic nerves stimulated. On each occasion five stimulations were made.
Therefore, two sets of measurements were made on separate occasions in each patient; in a supine position and with the patient sitting. There is evidence to suggest that diaphragm strength can be expected to fluctuate in the postoperative period after coronary artery surgery.21 Therefore, no attempt was made to directly compare measurements made in the supine and sitting up positions.21 Instead the aim was to determine if TwPet could be a useful indicator of TwPoes and hence TwPdi in either position. In addition, changes in lung volume have been shown to affect TwPoes more than TwPgas and so the relationship between TwPet, TwPoes, and TwPdi could also change over the same time period.18 However, it was possible to attempt to determine if a linear relationship existed between TwPet, TwPoes, and TwPdi in each of the two different positions.
The pressure traces were rejected if the baseline oesophageal or gastric pressure was distorted or if the twitch was imposed on a spontaneous or mechanical breath. The stimulations were 1 min apart. A small ramp of stimulations was made before the recordings to confirm that the stimulations were supramaximal or close to supramaximal.
Signal processing
Pressures were recorded via identical Validyne MP45 transducers (response range ±150 cm H2O) and amplified by Validyne carrier amplifiers (Validyne Corporation, Northridge, CA, USA). These were calibrated before each study with a Universal Pressure Meter (Bio-Tek Instruments Inc., USA), which was regularly checked for accuracy with a water manometer.22 The signals were passed to a 12-bit NB-MIO-16 analogue to digital converter board (National Instruments (NI), Austin, TX, USA), which had been installed within a MacIntosh Centris 650 computer (Apple Computer Inc., Cupertino, CA, USA). Pressure traces were analysed using programs based on LabView 2.2 software (NI).
Data collection
Pressure traces were inspected on line during the stimulation procedures to ensure they began on a steady baseline pressure at end-expiration. Twenty-two pressure traces were deemed unsatisfactory on subsequent off-line analysis and so excluded from the study (11 in the sitting position and 11 supine). Therefore, a total of 118 pressure traces out of a possible 140, all demonstrating Pet, Poes, Pgas, and Pdi in a total of 14 patients, were included in the analysis.
Statistical analysis
The statistical analysis was performed using Statview 4 (Abacus Concepts Inc., Berkley, CA, USA), and included linear regression, Wilcoxon Sign Rank tests and Bland and Altman plots.23
To allow a comparison of the ratios between TwPet, TwPoes, and TwPdi linear regression was used. The regression equations were also calculated with no intercepts, that is, made to pass through the zero point on both axes to allow the ratio between the variable on the ordinate and the abscissa to be calculated. Wilcoxon Sign Rank tests were used to compare TwPoes and TwPet.
In order to assess the agreement between TwPet and TwPoes we calculated the differences between the means of each of the five stimulations. The mean of these differences is a measure of accuracy or bias whilst the standard deviation (SD) is a measure of precision as presented in Figure 3. Both bias and precision are necessary to assess agreement.24 We calculated the limits between which 95% of the differences would lie (limits of agreement, 2 SD).23 We also calculated the mean and standard deviation of the ratio of mean TwPet: mean TwPoes to enable us to compare the values of the two methods over the range of twitch pressures observed (Table 1).
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To assess the spread of data between individuals, the coefficient of variation of TwPoes/TwPet and TwPet/TwPdi were calculated for each position to see if results became more variable in a given posture. TwPgas cannot be measured from mouth or tracheal tube pressures, but if it is a constant fraction of TwPdi in a particular posture, then this would imply that information relating to TwPoes alone may be enough to estimate TwPdi. However, if TwPgas is not a constant fraction of TwPdi, or if this is more of a problem in a particular posture, then estimates of TwPdi will be less reliable. To assess this we calculated the coefficient of variation of mean TwPoes/TwPdi between and within subjects for each posture.
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Results |
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The mean difference between TwPoes and TwPet measured in the supine position was 1.8 cm H2O (SD 2.2) (Fig. 4). As TwPoes and TwPet increased, the difference between the two methods also increased.
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In order to standardize for the wide range of measured pressures and to better explore these changes, we expressed them as a ratio of TwPoes/TwPet (Table 1).
The 95% confidence intervals for the likely differences (TwPoes TwPet) between the two techniques over a range of TwPoes from 2 up to 17 cm H2O in the sitting and supine positions was 5.3 to +1.8 cm H2O sitting and 6.2 to +2.6 cm H2O supine. However, the difference between TwPet and TwPoes was less than ±1 cm H2O at twitch pressures less than 8 cm H2O when supine and 10 cm H2O when sitting, and then became greater at higher pressures (Fig. 4).
TwPet was linearly related to TwPoes in both postures. In the sitting position TwPet was related to TwPoes r2=0.93 and TwPdi r2=0.65 (P<0.01). In the supine position TwPet was related to TwPoes r2=0.84 and TwPdi r2=0.83 (P<0.01). TwPoes was less than TwPet.
Variability
The within occasion coefficient of variation for supine measurements within individual patients was: TwPet 11.6%, TwPoes 14.6%, and TwPdi 11.8%. When sitting the results were similar: TwPet 13.5%, TwPes 13.9%, and TwPdi 11.2%.
The variability of between subject comparisons of TwPoes/TwPet, TwPoes/TwPdi, and TwPet/TwPdi are listed in Table 2 for both the supine and sitting postures. The ratio TwPoes/TwPet was slightly closer to 1.0 in the supine position although the between individual variability of this relationship was greater. On the other hand TwPoes made up a greater fraction of TwPdi supine and TwPoes/TwPdi was more consistent. When TwPet was related to TwPdi variability was relatively high and similar in both positions.
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TwPet, TwPoes and TwPdi supine
In the supine position mean values for TwPet were 26% greater than TwPoes (P<0.001, Wilcoxon Sign Rank test). When assessed using linear regression with no intercept, TwPoes made up 85% of TwPdi when supine and TwPet was equal to 105% of TwPdi when supine (Table 3). Therefore, the value for TwPet was a larger fraction of the TwPdi measurement in the supine position compared with the sitting position.
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Discussion |
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Factors affecting the transmission of pressure to the oesophagus and airway
TwPet was generally higher than TwPoes. Similar results have been seen in previous studies, when twitch mouth pressures were compared with TwPoes. When positioning the balloon catheters in the ICU after cardiac surgery, we could not achieve perfect 1:1 matching of Poes/Pet during a gentle inspiratory manoeuvre against a closed mouthpiece (mean 0.91 (SD 0.09)). Baydur studied normal subjects in laboratory conditions and could not always achieve a 1:1 relationship, particularly in the supine position, where he achieved an average of 0.96, ranging between 0.86 and 1.1. In practice, our mean of 0.91 could explain why our estimate of Poes compared with airway pressure would differ by 9%. This factor could help explain why TwPet is often slightly larger than TwPoes and probably contributes to the greater coefficient of variation of TwPoes/TwPet when supine (19.7%), compared with 11.4% in the sitting position. Indirect evidence from 133Xe ventilation studies suggested that in supine subjects there might be a gradient of pressure change in the pleura extending from the apex to the base compared to the airway. This may account for some of the difference between Pet and Poes in the supine position.25 26 Hamnegard found some instances of twitch mouth pressure (TwPmo) exceeding TwPoes in normal subjects.10 He postulated that the change in TwPmo may more accurately reflect average change in pleural pressure throughout the whole thorax during phrenic stimulation. The same could apply to TwPet measurements.
The difference between TwPet and TwPoes does become more prominent as twitch amplitude increases. This may be a problem of transmission of pressure to the oesophageal balloon, which is more difficult in the supine position.16 This is also a result of the weight of the heart and mediastinum which compress structures especially the lung, so disturbing the transmission of pressure to the oesophagus. This is even more likely after cardiac surgery when posterobasal atelectasis is extremely common. This makes it difficult to find a position where Poes reflects mean pleural pressure. Therefore, it may be that Poes measured with balloon catheters in these subjects when supine tend to underestimate mean pleural pressure change and TwPet may in fact be a closer estimate.
On the other hand, in patients with abnormal lungs with areas of slow time constants and with intrinsic positive end expiratory pressure (PEEP) it might be expected that TwPet would be less than TwPoes, because of failure of pressure transmission, rather than the opposite.
Cardiac contractions cause 12 cm H2O reductions in the magnitude of Poes in our experience. This feature is more prominent when supine (mean 3.5 (SD 1.8) cm H2O according to Baydur)16 and can be seen distorting the TwPoes in Figure 1. This will contribute to the relative reduction in TwPoes compared with TwPet on those occasions when the contraction coincides with the stimulation.
Clearly glottic closure is not a problem in intubated patients, although activation of some of the laryngeal musculature could occur during magnetic stimulation. This might lead to conformational changes in the airway or alter the position of the tracheal tube or its cuff so affecting TwPet. The importance of these factors remains to be quantified.
Some of our TwPdi data in this paper suggest the presence of varying levels of diaphragm weakness (mean TwPdi 11 (SD 4.7) cm H2O). Our recordings are made after cardiac surgery, which can be associated with phrenic nerve injury or diaphragm weakness. Previous estimates of the incidence of diaphragm dysfunction made slightly later in the postoperative period vary widely.2729 Some of our previous data,21 looks at the first 24 h after cardiac surgery, and does appear to show a higher incidence of diaphragmatic weakness (approximately 50% at 12 h), when compared with Polkeys normal data (normal mean TwPdi 26.8 (SD 5.5) cm H2O).30 31 This gradually improved over time. The resulting spread of strength levels is helpful, as it allows us to examine the techniques performance over a range of pressures.
The effect of recent wiring of the sternum on lung mechanics is also difficult to predict. Whether the process of opening and spreading the rib cage affects the intercostal nerves is unknown. The impact on the mechanics of the chest wall could alter chest wall compliance. This in turn would alter the impact that contraction of the diaphragm would have on the ratio of TwPoes/TwPgas, and so alter partitioning. However, this is not evident when our partitioning data is compared with previous work.9 11 Pain might affect the pressures produced during voluntary efforts, but this is less likely during non-volitional stimulations such as used in this study.
The effect of the contribution of TwPoes and TwPgas to TwPdi
TwPet may be a reflection of the TwPoes component of TwPdi, which forms a larger fraction of TwPdi as we move towards the supine position. Conversely there is a large TwPgas contribution to TwPdi, when sitting, which is not reflected in the TwPoes or TwPet response to diaphragm stimulation. This may explain the lower r2 value for the association of sitting TwPet with TwPdi and sitting TwPoes with TwPdi. To compound this problem, the fraction of TwPdi made up by TwPoes compared with TwPgas differs greatly between individuals, as seen from the coefficient of variation between individuals of TwPoes/TwPgas: 12.8% supine and 18.9% sitting. Therefore, TwPet may reflect TwPoes, but as TwPoes forms a different fraction of TwPdi in each individual, especially when sitting, and does not reflect the TwPgas component of TwPdi, TwPet while sitting has some limitations in its ability to indicate TwPdi.
We have been able to generate linear equations that allow the prediction of TwPdi from TwPet, but the accuracy of prediction will always be hindered by the lack of a TwPgas measurement and the lack of knowledge of partitioning in that individual. However, as the coefficient of variation of partitioning between occasions within an individual from longitudinal studies is less than 10%, serial measurements of TwPet may still be an effective means of recording changes in diaphragm strength over time for that individual.
In summary, TwPet combined with BAMPS does reflect TwPoes in response to diaphragmatic stimulation, particularly at low strength levels, allowing an estimate of TwPdi from the TwPet measurement, especially when making supine recordings. This may be a useful means of detecting patients with reduced diaphragm contractility who could then be tested further, by more invasive and potentially more precise techniques.
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References |
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