BJA Advance Access originally published online on February 20, 2006
British Journal of Anaesthesia 2006 96(4):510-515; doi:10.1093/bja/ael035
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Respiratory muscle activity and respiratory obstruction after abdominal surgery
University Department of Anaesthesia, Critical Care and Pain Medicine Royal Infirmary, Edinburgh EH16 4SA, UK
*Corresponding author. E-mail: g.b.drummond{at}ed.ac.uk
Accepted for publication January 18, 2006.
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Abstract |
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Background. Respiratory movements in patients after abdominal surgery are frequently abnormal, with associated disturbances in the pattern of inspiratory pressure generation. The reasons for these abnormalities are not clear and have been attributed to impaired action of the diaphragm. However, an alternative is that partial airway obstruction could trigger reflex activation of the inspiratory ribcage muscles, which would cause a similar pattern of inspiratory pressure change. Direct measurement of electrical activity can indicate if reflex activation of inspiratory muscles occurs when partial airway obstruction is present.
Methods. In an open study, we implanted electrodes to measure the EMG of scalene, intercostal and external oblique abdominal muscles in patients after lower abdominal surgery. Analgesia was with morphine i.v. by patient control. We used nasal cannulae to measure nasal airflow and compared EMG activity when airway obstruction was present with activity when breathing was not obstructed.
Results. The pattern of activity of the different muscles was distinct. Intercostal activity reached a maximum during inspiration, before the scalene muscles, whereas scalene activity increased in phase with increasing lung volume. Abdominal muscle activity commenced when expiratory flow had ceased and continued until the next inspiration. In all three muscle groups, partial airway obstruction did not alter muscle activity.
Conclusions. Partial airway obstruction does not activate inspiratory ribcage muscles, in patients receiving morphine for postoperative analgesia after lower abdominal surgery. Changes in respiratory pressures and abnormalities of chest wall movement described in previous studies cannot be attributed to reflex responses and probably result from increased airway resistance and abdominal muscle action.
Keywords: airway, obstruction; muscle respiratory; ventilation, postoperative
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Introduction |
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In patients after abdominal surgery, respiratory movements are commonly abnormal. Ribcage movements with inspiration are proportionally greater and abdominal movement is small or even paradoxical. Breathing is generally more rapid and shallow, although this can be slowed by opioid analgesia. In a previous study,1 we measured respiratory movements and gastric and abdominal pressures in patients overnight after upper abdominal surgery. Abnormal patterns occur when phasic activity of the abdominal muscles is present during expiration and this activity reduces the change of transdiaphragmatic pressure during inspiration. As the proportion of transdiaphragmatic to pleural pressure change is altered, some authors suggested that the function of the diaphragm was impaired after surgery.2 This suggestion derived from an analysis of inspiratory muscle action alone and did not consider the effects of expiratory muscle action.3 An extension of this analysis suggests that abdominal muscle action, during expiration, can generate pressure changes that resemble those of the rib cage inspiratory muscles.2 The ribcage muscles, acting alone during inspiration, reduce the pressure in both the pleural and abdominal cavities, pull in the abdominal wall and expand the ribs. The abdominal muscles, acting alone in expiration, increase the pressures in both cavities and the abdominal wall is pulled in, as the diaphragm is forced up. The motion of the ribcage depends to a great extent on activity of the lower intercostal muscles that may or may not accompany abdominal muscle activity. Thus, measurement of these pressures and the associated chest wall movements, cannot reliably distinguish between these alternatives, of rib cage inspiration or active expiration generated by abdominal muscle contraction.
The factors that trigger abdominal muscle activity are not fully understood, but activity is more frequent when airway patency is impaired.4 However, in addition to this response to airway obstruction, the ribcage muscles are affected by muscle spindles which regulate the reflex control of muscle length.5 6 It is therefore possible that airway obstruction could reflexly activate inspiratory intercostal muscles.7 Action of either muscle group—inspiratory activity of the ribcage, or action of the abdominal muscle during expiration—could be responsible for the changes seen in our previous study.1 Using direct measurements of respiratory muscle activity, we set out to examine the specific possibility that intercostal activation was caused by airway obstruction and thus could explain the abnormal breathing patterns we have reported.
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Methods |
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After ethical approval, we obtained written informed consent from patients who were about to have elective abdominal surgery for non-malignant gynaecological conditions and were planned to receive i.v. patient controlled analgesia with morphine for postoperative analgesia.
We did not exclude any patients for medical reasons. Anaesthesia was not strictly standardized, but in all patients anaesthesia was induced with propofol and maintained with isoflurane, nitrous oxide and i.v. morphine, with either atracurium or vecuronium for neuromuscular block. After surgery was complete, the neuromuscular blocking agent was antagonized with neostigmine and the patient was allowed to breathe spontaneously, while still anaesthetized. During this time we inserted electrodes in three muscles: the middle part of the right middle scalene, the intercostal muscle in the third right intercostal space, approximately 3 cm lateral to the sternal edge, and the right transversus abdominis, 4 cm inferior to the costal margin, and just lateral to the margin of the rectus abdominis. We applied antiseptic solution (Betadine) to the skin over the relevant muscles and used a 23 gauge hypodermic needle to insert sterile silver wire electrodes, 10 cm long and 0.2 mm in diameter, insulated with PTFE except for 5 mm at the end. The end 4 mm of the wire was bent over and inserted into the needle opening. The wire and needle were inserted together through the skin and into the muscle. To guide insertion into the scalene muscle, the muscle was palpated. To assist placing the wire accurately in the intercostal and abdominal muscles, we obtained an image of the muscle layers with a portable ultrasound apparatus (Site-Rite, Jade Medical, Tilehurst, Reading, UK). As the needle was withdrawn, pressure was applied to the skin over the needle tip, so that the wire remained in place. We inserted three electrodes in each muscle and taped them securely to the skin surface.
We studied each patient between 2 and 5 h after return to the ward. Patients were studied lying supine with their head on a pillow. We connected pairs of wires from each muscle to an isolated preamplifier (Neurolog NL 820). The signals were then amplified and filtered with a bandwidth of 30 Hz to 3 kHz (Neurolog NL 106/125) and rectified and integrated with a time constant of 200 ms (Neurolog NL 703). (Neurolog products were from Digitimer Ltd, Hertfordshire, UK.) We placed a fine cannula in the nostrils to measure gas flow (Protek Medical Products, Inc., Iowa City, IA, USA) and a single inductance band (Respitrace, North Bay Village, FL, USA) around the ribcage immediately below the axillae to measure respiratory movement.
The electrical signals were digitized at 100 Hz using an analogue to digital converter (CED1004) and recorded with a personal computer using a commercial software system (Spike 2), both from Cambridge Electronic Design, Science Park, Cambridge, UK. Further data analysis was with GraphPad Prism version 4.00 for Windows (GraphPad Software, San Diego, CA, USA, www.graphpad.com).
In each patient, we recorded airflow, ribcage movement and two EMG channels simultaneously, because we were limited to four channels of simultaneous recording. To record all the EMG signals, we then recorded flow, movement and two further EMG signals. The raw EMG was continuously observed on an oscilloscope to ensure satisfactory signals. A pulse oximeter reading was observed continuously in all subjects. After recording, the nasal flow signals were replayed separately and breaths chosen and marked as being obstructed or unobstructed according to the criteria used in a previous study.8 Briefly, obstructed breaths were identified by reduced flow, a flattened time profile and as those preceding ‘recovery’ of airway patency, signalled by a sudden increase in flow. A paired obstructed and unobstructed breath was chosen within 10 respiratory cycles, so that the possibility of a change in electrode characteristics, affecting the size of signal, was reduced. We took care not to sample the larger breaths that accompanied respiratory arousal. In addition, the entire duration of study was of no more than 15 min to reduce the possibility of a time-related change in respiratory drive or electrode characteristics. The EMG traces were then replayed while masking the airflow and ribcage signals, and the amplitude of the integrated EMG signal for each of the marked breaths was measured. The median amplitude for each patient, muscle and state was calculated and the signal amplitude for the obstructed state was expressed as the ratio of the amplitude measured for clear breathing, for each patient and muscle site.
We also measured the duration of inspiration and expiration for each of the measured breaths, using the flow signal.
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Results |
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We approached 20 patients for permission, received permission from 16 and obtained successful recordings in 14 patients of age 42 (21–61) yr [mean, (range)], height 158 (9) cm and weight 66 (6) kg [mean, (SD)]. The mean BMI was 27 kg m–2 and the range was from 20 to 30. The mean dose of morphine given during surgery was 13 (6) mg and the dose of morphine administered from the PCA from the end of surgery to the time the study started was 16 (11) mg [mean (SD)]. The breathing pattern in these patients was variable, and proportion of breaths identified as obstructed varied from patient to patient. The average proportion of breaths identified as obstructed in each subject was 47% (SD 18), but this varied considerably from 10 to 73%.
The success in recording satisfactory signals varied for each muscle. Satisfactory signals were obtained from the scalene muscles in all patients, from the abdomen in 13, but reliable intercostal signals were only obtained in 7 patients. Because the proportion of obstructed and unobstructed breaths varied from patient to patient, the total numbers of measures of amplitude varied. The average number of individual breaths used for a median estimate of EMG amplitude was between 6.9 and 8.3 breaths per patient. All patients studied were breathing oxygen and all had a satisfactory pulse oximeter saturation value >93%.
A good example of an integrated EMG tracing is shown in Figure 1. The EMG signal from the intercostal muscle was typically symmetrical, showing activity, which increased shortly after the nasal flow signal, and then declined from a maximum before the onset of expiration. The scalene signal lagged behind the intercostal and only started to decline at about the start of expiration. Because the duration of expiration was often long and variable, the pattern of the abdominal EMG was very variable. The example shown is typical: onset of activity is seen shortly after expiratory flow ceases, and not during the period of expiratory flow itself. If expiration was prolonged, then activity continued as a plateau, maintained as long as the expiratory pause continued, followed by a decline in activity at the onset of the next inspiration. Figure 1B also shows a typical partially obstructed inspiration, as the first inspiration in the series.
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The relative duration of obstructed and unobstructed breaths, expressed as the duration of inspiration, and expiration, is shown in Figure 2. There was no statistically significant difference between these times. The ratio of peak activity for the obstructed and unobstructed breaths is shown in Figure 2B. The ratio was 1.01 (0.71–1.31), 1.10 (0.89–1.32) and 0.94 (0.69–1.18) (average, 95% CI), respectively, for scalene, abdominal and intercostal activities. There was no significant difference from 1 for any of these ratios (Wilcoxon test). However, the distribution of the ratios, particularly for the abdominal activities, was not normal, so the ratio data were transformed into logarithms to allow further statistical analysis. There was no significant difference from 1 (Student t-test). The approximate power of the measures in detecting a difference of 0.3 (i.e. a 2-fold change in peak activity) was more than 80%.
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Discussion |
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We could not find any difference in the activity of the respiratory muscles when we compared partially obstructed and unobstructed breath cycles, and conclude that reflex increases in ribcage muscle action, in response to partial obstruction, are unlikely to account for previous observations. In fact, our finding that phasic abdominal muscle activity is easily detected in these patients after abdominal surgery supports our previous suggestion, that abdominal muscle activity generates these variations in abdominal and pleural pressure. We suggest that changes in transdiaphragmatic pressure are less than expected because the abdominal muscles increase transdiaphragmatic pressure during expiration, by generating passive tension in the diaphragm as the abdominal pressure increases. Consequently, at the onset of inspiration, this pressure is already increased and decreases when the abdomen relaxes, only to increase again as the diaphragm contracts.
Some practical aspects of this study require consideration. Nasal prongs9 are an effective and sensitive means of measuring nasal flow, and can accurately detect increased resistance to flow.10–12 From this previous work, and our previous study8 we are confident that we can distinguish reliably clear and obstructed breathing. The recognition of a period of sub-total airway obstruction is simplified by the pattern of acute resolution, with a sudden and prominent increase in nasal flow that is very typical.8
Integration of the EMG provides a method of quantifying muscle activity13 which is linearly related to muscle force when the contraction is isometric.14 15 However, when muscle shortening occurs, or the relationship between length and tension is affected by changing the load on the muscle, then the relationship between force and EMG activity is altered.16 However, the EMG signal indicates the degree of activation of the muscle by its neural input.17 We were unable to record parasternal intercostal activity as reliably as the other muscles. Despite ultrasound imaging, accurate placement in these thin muscles proved difficult. Nevertheless, the close relationship in overall activity between scalene and intercostal muscles suggests that the scalene findings were a satisfactory measure of overall inspiratory ribcage muscle action.17 18
The actions of the intercostal muscles are not uniform. The parasternal muscles are predominantly inspiratory.19 Of the intercostal muscles, the more cranial are inspiratory, and the more caudal expiratory. The scalene muscles stabilize the upper ribcage and are important inspiratory muscles.20 21 They act with other muscles such as the sternomastoid22 and can contribute substantially to the inspiratory force during maximal manouevres.23 When respiration is stimulated, the increase in activation of the accessory muscles is much less than the diaphragm,17 indicating the secondary role that these muscles play in contrast to the important pumping role of the diaphragm. When loads are imposed, ribcage muscles are recruited.24 Even briefly applied loads cause activation.25 In conscious subjects, when inspiration is transiently occluded, reflex inhibition is followed by augmentation of inspiratory chest wall muscles. In normal subjects there is a 44% increase in activity in response to a 250 ms occlusion,26 which is probably mediated by afferents from the intercostal muscles.27 On the other hand, tension receptors in diaphragm can inhibit the intercostals, particularly the external intercostals.28 This observation is relevant because abdominal muscle activation during expiration will increase passive diaphragm tension and could thus inhibit intercostal activity, which in the lower rib cage is predominantly expiratory. In this way, an increase in abdominal pressure may generate an inspiratory effect on the rib cage by an outward pressure via the zone of apposition,29 unopposed by the constrictive effects of the lower intercostal muscles. Another potential reflex, described in dogs, is that although inspiratory occlusion can reflexly activate levator costae and external intercostal muscles, as we hypothesize, the parasternal intercostals are inhibited, by a vagal reflex.7
An important consideration in interpreting our observations is to estimate the degree of activation of the intercostal and scalene muscles needed to generate the pressure changes noted during inspiration in patients after abdominal surgery. This is not simple, as the pressure changes that occur are exaggerated by increased airway resistance, so that the muscles are less able to shorten, and thus they develop greater pressure. However, we found that gastric pressure was about 3 cm H2O less positive at the end of a partially obstructed breath.1 A similar magnitude of change was noted between before and after surgery in a study by Sharma and co-workers.30 This pressure change would require nearly maximal activation of either the parasternal intercostal muscles31 or the scalene muscles.23 Because the inspiratory ribcage muscles are additive in expanding the ribcage,22 then a decrease in gastric pressure of this size would indicate an approximately half maximal activation for both the muscles. This degree of activation is at least four times the activity seen in a normal quiet breath,20 and we would expect to see a log ratio of 1.6. The upper 95% CI of the values we observed was 1.3. Thus the degree of inspiratory rib cage muscle activation required to generate such pressure swings is clearly not consistent with the degree of activation that we observed, even when the muscle activity was increased, as it was in some subjects.
The duration of inspiration of the obstructed breaths did not differ from the unobstructed breaths. This is very relevant to the interpretation of the relative amplitudes of the obstructed and clear breaths. If the duration of the obstructed breath was shortened, then a reflex increase in the rate of activation could have occurred, but would have been concealed if the inspiration ended sooner than the normal breath.
Finally, it is possible that when the clear breaths were being taken, the chemical drive to breathing was less than it was during partial obstruction. If this possibility were present, the drive from the respiratory centre would be less, and the amplitude of the unobstructed breaths would be reduced. Thus, if the obstructed breaths were larger, there would be two possible explanations: increased stretch reflex activation, or stimulation by hypercapnia. Presumably the reason this second influence did not increase the obstructed breath activity was either because morphine analgesia had reduced chemosensitivity, or more likely there were only minimal differences in carbon dioxide chemostimulation because the intervals between the breaths were small.
We noted considerable and consistent abdominal muscle action. This increased activity was very similar to that noted in previous studies,1 32 although those were patients after upper abdominal surgery. The similarity of the abdominal EMG in these studies suggests that the current observations can be applied to most patients with an abdominal incision and receiving systemic opioid analgesia. Much of this increase appears to be the effect of opioid analgesia as it was not noted in some patients in a study where analgesic treatment did not include opioids.30 Opioids increase abdominal muscle activity33 34 but the exact mechanism is unclear.35
We conclude that reflex activation of the ribcage muscles by airway obstruction is not present in patients after lower abdominal surgery, and cannot explain previous observations of large decreases in pleural pressure during partial obstruction.
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