and abdominal cavities. The relative changes in Pab and Ppl should indicate the relative contributions of these inspiratory muscle groups, the diaphragm and.
“I would have everie man write what he knows and no more.”—MONTAIGNE
BRITISH JOURNAL OF ANAESTHESIA VOLUME 80, No.3
MARCH 1998 EDITORIAL I Diaphragmatic dysfunction: an outmoded concept
The expression “diaphragmatic dysfunction” is a mellifluous phrase used when considering the respiratory changes associated with major surgery.1–5 A recent editorial in this journal concerning the effects of laparoscopic cholecystectomy6 discussed inhibition of diaphragm function, modified breathing patterns and changes in the abdominal contribution to breathing attributed to reflex diaphragmatic inhibition: all of these concepts have been considered to represent diaphragmatic dysfunction. However, some articles have voiced muted doubts about the concept,7–9 which I believe is now sufficiently threadbare to require that the expression be used rarely, if at all, when we consider changes in respiratory pattern after abdominal surgery. The expression was first used by Ford and co-workers in an article entitled “Diaphragm function after upper abdominal surgery in humans”.10 They applied the theory that diaphragm contraction and descent during inspiration not only generates a decrease in pleural pressure (Ppl), but also an increase in abdominal pressure (Pab). In contrast, if an inspiration is generated by the intercostal muscles acting alone, abdominal pressure decreases. This decrease is the same as the decrease in pleural pressure because the diaphragm is inactive and does not establish a pressure difference between the pleural and abdominal cavities. The relative changes in Pab and Ppl should indicate the relative contributions of these inspiratory muscle groups, the diaphragm and ribcage muscles to inspiratory activity.11 If Pab changed less, relative to the change in pleural pressure during inspiration, then a “dysfunction” of the diaphragm was present. This analysis is confounded when the abdominal muscles are active. Abdominal muscle contraction followed by relaxation can generate relative changes in Pab and Ppl very similar to intercostal activity (fig. 1). The effect of abdominal muscle activity was generally discounted by early investigators. Studies employing this analysis have used different means of expressing the relative changes in Pab, Ppl and trans-diaphragmatic pressure (Pdi), which is calculated from the two preceding values, thus: Pdi : Pab 9 Ppl. The most frequent expressions used are Pab/Ppl (which is awkward because the denominator has a negative value) and Pab/Pdi (which is mathematically related, being 1/(1 9 Ppl/Pab)). Most studies reported that the pressure swings were measured from “maximum to minimum” values, irrespective of time, within a respiratory cycle, read from a chart recorder.10 12–15 However, it is evident from the theory
outlined that to provide an accurate indication of muscle contribution to inspiration, the pressure changes compared must be during the same period of inspiration. If the measurements include abdominal pressure changes during expiration, caused by abdominal muscle contraction, this affects the “maximum to minimum” estimates. Ford and co-workers suggested that the changes they reported “may be attributable to diaphragm dysfunction”.10 Further studies followed, with one using the term “diaphragmatic dysfunction” in the title.14 Such studies also used other indirect measures of diaphragm function, such as the relative motion of the ribcage and abdomen.16 Ford and co-workers have since reviewed the topic7 and are now more circumspect with the term “dysfunction”, preferring to describe a change from diaphragm to intercostal activity in a review of the extensive animal studies which support reflex inhibition via visceral afferent pathways. Unfortunately, the term “diaphragmatic dysfunction” is used when other plausible possibilities have been present. These included phasic activity of the abdominal muscles, which can cause abdominal pressure changes in addition to those changes generated by the diaphragm, and also causes of increased ribcage muscle activation.
Abdominal muscle activity The normal pattern of change in Pab is an increase during inspiration, with a decline during expiration. However, the abdominal muscles often become active in expiration, for example: in exercise; with impedance to inspiration17; in patients with obstructive airways disease18; and during anaesthesia.19 Abdominal muscles are also active in patients after surgery: their activity causes an additional phase of increasing abdominal pressure during expiration. This pressure subsides rapidly at the onset of the next inspiration. It can be greater than the pressure change in inspiration so that the usual increase in pressure associated with inspiration and contraction of the diaphragm can be swamped by a much greater pressure swing induced by abdominal muscle contraction.20 In the awake subject, this activity may be continuous, but during sleep or airway obstruction, phasic activity during expiration is more common. Early direct observations of abdominal muscle activity after surgery were later supported by studies which showed activity in patients after thoracotomy,21 cardiac surgery,8 abdominal surgery9 and transiently after laparoscopic surgery.22
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Figure 1 Schematic representation of the actions of respiratory muscle groups. A: Diaphragm contraction: the diaphragm descends, displacing the abdominal wall outwards. Pleural pressure decreases and the ribcage is pulled inwards by the increased pressure difference. B: Ribcage contraction: the ribcage is displaced outwards and pleural pressure decreases. The inactive diaphragm does not create a pressure difference and the abdominal pressure decreases in parallel with pleural pressure. C: Abdominal contraction: the abdominal wall moves in, increasing abdominal pressure and forcing the abdominal contents and the diaphragm cranially. Pleural pressure increases and lung volume decreases (expiration). Relaxation of the abdominal wall reverses these changes.
A plot of abdominal pressure and volume can show how the abdominal muscles are working.9 22 When abdominal pressure increases as a result of diaphragm action, the abdominal wall moves out: if the increase in pressure has been caused by abdominal muscle contraction, the abdominal wall either does not move (but may change its shape) or moves inwards if the diaphragm does not resist being forced upwards into the ribcage.
Activation of ribcage muscles The ratio of changes in abdominal and pleural pressure during inspiration reflects the degree of activation of the ribcage and diaphragm. After operation, the predominant effect may be an increase in ribcage muscle action. An increase in the proportion of drive to the ribcage muscles can result for several reasons. If there is an overall increase in drive, such as is common after surgery, then the proportional activation of other inspiratory muscles is likely to increase to a greater extent than that of the diaphragm.23 Even if overall drive does not increase, changes in airway resistance with sedation can lead to marked increases in ribcage movement,24 probably from a reflex increase in activity of the ribcage muscles, which are richly supplied with muscle spindles. Nimmo and Drummond found that patterns of pressure changes, consistent with increases in ribcage activity, were significantly related to airway obstruction.9 Clergue and colleagues8 concluded that increased ribcage muscle activity and phasic expiratory activity were responsible for the postoperative changes they described, with no convincing evidence of alterations in diaphragm activity. Finally, even with the same drive and relative intercostal activity, abdominal pressure changes are greater, and abdominal movements less, if abdominal compliance is decreased, for example by tonic abdominal activity.25
How can dysfunction of the diaphragm be defined and recognized? A simple definition is that a muscle is functioning less well if it fails to generate its normal tension for a given degree of electrical activation. In patients after abdominal surgery, this is not easy to demonstrate. Respiratory frequency increases and tidal volume is reduced after abdominal surgery.26 Consequently progressive activation of the diaphragm during inspiration is cut short more quickly, and the degree of activation at the end of inspiration is less than that before operation. Simple measures of activity at the end of inspiration are thus of no value in determining changes in diaphragm properties. Changes in electrical activity, such as those reported after extradural block in postoperative patients,27 could be attributed to changes in respiratory frequency that occur at the same time. When electrical activity was related to transdiaphragmatic pressure, extradural analgesia did not alter the relationship between electrical activity and pressure generated by the diaphragm, despite changes in other “indices of contractility” such as ⌬Pab/⌬Pdi. In five patients after abdominal surgery, direct maximal stimulation of the phrenic nerves, with measurement of the resultant diaphragmatic pressure, was used to assess any changes in diaphragm contractility. Although this study would have been technically difficult, the results suggested that there was no change in contractility.13 The remaining attribute of the concept of “diaphragmatic dysfunction” is of central inhibition of inspiration, caused by visceral pain. Limitation of vital capacity has long been recognized to accompany abdominal surgery, and to be more marked the closer the incision is to the diaphragm. More recently, laparoscopic intra-abdominal procedures have also been recognized to limit maximal inspiration, and this effect is more severe after cholecystectomy than lower abdominal procedures, suggesting that visceral
Editorial I damage is important.28 The exact neural pathways involved are not clear: extradural anaesthesia can only partly restore vital capacity, and the activity of the diaphragm on maximal voluntary inspiration is more suppressed than “semi-voluntary” maximal manoeuvres such as sniff.28 There are no data to indicate that inhibition of maximal inspiration is exclusive to the diaphragm. The concept of “dysfunction” led to interventions to reduce it. Two approaches were investigated. Aminophylline, which can improve muscle contractility in some circumstances, was given to patients after upper abdominal surgery.15 The example trace in this study shows that considerable abdominal muscle activity was present, with abdominal pressure increasing during expiration and suddenly decreasing at the start of inspiration. Aminophylline abolished this abdominal muscle action, converting the trace to one that resembled the preoperative pattern. Nevertheless, the authors rejected the possibility that abdominal muscle action was responsible for the changes they reported, on the grounds that the pressure swings were similar before and after operation, and suggested that administration of aminophylline improved the index ∆Pab/∆Pdi and thus improved diaphragm function. However, in experimental animals treated with aminophylline, direct measurements of diaphragm length did not show an improvement in diaphragm contractility,29 and another clinical study found an increase in maximal inspiratory effort that was probably a centrally mediated effect.2 It appears that aminophylline acts as an analeptic. Even if it were an effective therapy, it is unlikely to prove popular: it has a narrow therapeutic margin, several adverse effects and important interactions with other treatments used in postoperative patients.30 If diaphragm dysfunction is caused by reflex inhibition, then extradural block might interfere with the reflex and improve mechanics. Motor block of the abdominal muscles also has a potentially important effect on chest wall movement. Mankikian and co-workers studied the effects of thoracic extradural block to T4 obtained with 0.5% bupivacaine, using ∆Pab/∆Ppl and chest wall measurements.12 No electrical measurements of abdominal muscle activity were made, but activity was clinically evident in two of the 12 patients. The change in abdominal pressure was measured as “peak inspiratory minus peak expiratory pressure” so the expiratory pressure included contributions from abdominal muscles. Not surprisingly, the main effect of what was probably a large degree of abdominal motor block was a small increase in the abdominal pressure swing, and an increase in abdominal outward movement on inspiration. They concluded that diaphragm function had improved, although the probable abdominal muscle motor block makes this conclusion uncertain. A subsequent study from these workers27 recognized the problems of expiratory abdominal muscle action and incorporated changes in the measurements of the pressure swings to avoid the expiratory phase. They also measured diaphragm electrical activity and found no evident changes in contractility. Despite paradoxical breathing patterns, where the abdomen moved inwards during inspiration, the electrical
279 activity of the diaphragm persisted. They concluded that the diaphragm was inhibited by visceral pain and that extradural block removed the afferent stimulus causing this inhibition. In fact, the most prominent effects noted were a decrease in respiratory rate, an increase in tidal volume and a greater outward movement of the abdomen, all of which could result from abdominal sensory and motor block. More invasive studies did not reveal important changes in diaphragm function. Fratacci and colleagues21 studied the effects of thoracic extradural block in a small number of patients after thoracotomy, in whom sonomicrometre crystals had been implanted to measure changes in diaphragm length. Extradural analgesia did not improve contraction: indeed paradoxical lengthening occurred in three patients. The authors suggested that the ribcage muscles were contracting more strongly. However, a representative trace obtained before extradural block revealed an increase in gastric pressure towards the end of expiration. This pressure would act to lengthen the inactive fibres of the diaphragm in expiration, which would subsequently tend to shorten when the abdominal muscles relaxed at the onset of inspiration. Thus an alternative explanation for the paradoxical effect of extradural anaesthesia would be abolition of the lengthening in expiration, and hence less “shortening” action during inspiration. A general criticism that can be levelled at many of these studies of postoperative patients is that they were made over only short time periods, and may not have been entirely representative. Longer recordings show frequent changes in respiratory pattern, with abnormalities developing and disappearing, sometimes quite quickly. Abnormal breathing patterns are significantly related to airway obstruction.9 Considering the complex interactions of the respiratory muscles, to expect that the action of the diaphragm could be analysed and assessed with a single simple measurement was unrealistic. The uncritical application of the concepts of abdominal and pleural pressure change associated with diaphragm action, in clinical circumstances where the other respiratory muscles are acting, often powerfully, has stimulated a lot of research, and a cloud of misconception. Now, with more careful study, the clouds are clearing, but the view is far from simple. Clearly, the abdominal muscles have an important role in the breathing pattern of the patient after abdominal surgery. It is not evident if the abnormalities in breathing, of themselves, require treatment, or how they could be altered if this were desirable. These changes in respiratory mechanics could conceivably be an appropriate and effective response to surgical trauma.7 However, lung collapse and infection remain difficult problems for patients after abdominal surgery, and abnormalities in abdominal muscle activity may contribute to them: careful clinical physiological measurements and clear thinking are needed to tease out the links and develop effective therapies. G. B. DRUMMOND Department of Anaesthetics Royal Infirmary Edinburgh EH3 9YW
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