The early restoration of spontaneous breathing is of decisive importance, as we know, on the outcome of resuscitation. When it is revived quickly, there is complete and stable restoration of all the organism’s functions that have experienced clinical death. But it is delayed, the organism dies or becomes ‘decorticated’. That is one of the fundamental conclusions of reanimatology.
To restore the activity of the respiratory centre when withdrawing the organism from a terminal state, it is above all necessary to restore circulation in the region of the medulla oblongata. In addition to the measures for restoring cardiac activity, in order to restore gas exchange in the lungs it is necessary to begin artificial respiration as soon as possible. In this it is not only the restoration of normal gas exchange in the lungs that is important but also, at a certain stage of resuscitation, reflex stimulation of functioning of the respiratory centre through the Hering-Breuer reflex. In addition to the Hering-Breuer reflex, spinal reflexes radiating from the proprioceptors of the respiratory muscles are of importance in reflex stimulation of breathing.
The role of spinal reflexes that end in the motor neurons of the spinal cord has been demonstrated in experiments in slitting the spinal cord at the first cervical vertebra. Inflating the lungs by artificial respiration in ‘spinal’ animals showed that the greater the volume of each inhalation, the stronger was the reflex contraction of the respiratory muscles. The sooner artificial respiration is begun, the sooner spontaneous breathing begins; and, as mentioned above, the prognosis of resuscitation greatly depends on this. A necessary condition for restoring the functions of the cerebral cortex is the revival of a focus of stimulation in the medulla oblongata.
The respiratory centre of the medulla oblongata is one of the main sources of the genesis of the background electrical activity of the higher sectors of the brain. The impulses that radiate from it promote the development of the earliest forms of electric activity of the cortical-subcortical formations and are capable of strongly modifying their own rhythm. It has been shown that, although the respiratory centre, like all sources of efferent impulsation, is one of several ‘drivers’ of brain rhythms, it is of prime importance owing to its links with the whole nervous system and to the constancy and rhythm of its activity.
Renewal of circulation, as we know, is the basic condition for restoring functioning of the higher sectors of the brain, but it is still insufficient for rapid restoration of the cortex and subcortex. It is necessary that the focus of stimulation in the medulla oblongata that arises during restoration of physiological functions has to ‘rouse’ the cortex. Irradiation of stimulation from this region in the cerebral cortex acts as a powerful pacemaker for the subcortical formations, and subsequently for the cortex. Thus it is clear why early restoration of spontaneous breathing, which is at once an index of the reactivation of the bulbar region, decides the outcome of resuscitation.
The enormous role played by restoration of respiration in the outcome of resuscitation, of course, is persuasive of the need to pay more attention to study of the dynamics and features of the extinction and restoration of external respiration.
As research has shown, the changes in respiration during dying have a phased character. In experiments on dogs that had died from loss of blood, analysis of pneumograms revealed a phase of quickened respiration, one of slowing, a terminal pause in breathing, and agonal breathing.
Study of the electrical activity of the respiratory muscles, the electromyogram (EMG), has great significance because, besides giving an evaluation of the apparatus of external breathing, it makes it possible indirectly to estimate the functional state and organization of the respiratory centre in various conditions of the organism’s vital activity.
The special research carried out in our laboratory to study the structure of the respiratory act from the bioelectric activity of the respiratory muscles of dogs during dying from massive blood loss and subsequent reanimation showed that the amplitude of the oscillations of the biocurrents of the inspiratory muscles increased at the beginning of bleeding while in expiratory muscle activity developed. When exhalation was also active in the initial state the amplitude of the oscillations of the biocurrents in the expiratory muscles increased during bleeding. The accessory muscles developed phasic activity during inhalation on a background of tonic activity. The increase in the activity of the respiratory muscles in the phase of quickened breathing leads on average to a 60 per cent increase in minute volume. At the same time disynchronization of cortical electrical activity is observed on the electrocorticogram.
When breathing slows down, as arterial pressure falls, slow waves appear on the electrocorticogram, the pupillary reflexes disappear, and the corneal reflexes become listless, while the inspiratory and accessory respiratory muscles maintain clearly expressed electrical activity. The expiratory muscles contract during exhalation and during the respiratory pause. Pulmonary ventilation in this phase is 60 per cent of the initial volume.
At the end of the phase of slow breathing before the terminal pause, when cortical electrical activity ceases, the amplitude of oscillations of biocurrents of inspirator muscles drops, and expirator activity disappears, but marked bursts continue in the accessories during the inhalatory phase.
During agony the pneumogram shows breathing in the form of gasping or weak superficial breathing. During either gasping or weak superficial breathing a disturbance of reciprocity between inspirators and expirators is seen on the EMG of the respiratory muscles; in the inhalation phase the expirators contract at the same time as the inhalators and accessory muscles.
The simultaneous contraction of expiratory and inspiratory muscles is apparently the result of irradiation of impulses from the highly excited inspiratory centre to the expiratory centre. During agony the excitation of the respiratory centre irradiates to the motor neurons of other skeletal muscles; hence, practically all the muscles of the body and extremities contract at the same time as the respiratory muscles in the inhalatory phase.
The efficiency of external breathing is very low during agony, the minute volume being only 15 per cent of normal, probably because the expiratory muscles, i.e. the muscles of the anterior abdominal wall, in contracting together with the inhalators, hamper the movement of the diaphragm, which is the main inspirator muscle and, according to Wade, accounts for three-quarters of respiratory volume.
From analysis of our experimental data, plus that in the literature we concluded that the reason for the development of agonal breathing was not only hypoxial cessation of central control of the medullary respiratory centre but also the greater or lesser degree of hypoxic alteration of the brain stem apparatus.
During resuscitation breathing is restored after different times depending on the duration of circulatory arrest. From electromyograms of the respiratory muscles during the restorative period, three types of normalization of the structure of the respiratory act are distinguished.
The first type is observed in experiments with clinical death of three to five minutes duration and relatively early restoration of the main vital functions, in which cardiac activity develops during the first minute, respiration during the first three minutes, and corneal reflexes during the first 12 to 14 minutes after the beginning of resuscitation. With restoration of breathing the EMG registers bursts in the inhalatory phase in the inspiratory and accessory muscles. In expiratory muscle electrical activity develops on average nine minutes after breathing is restored. This activity revives at the very beginning of inhalation, then, at the end of the respiratory pause, gradually seems to ‘shift’ toward the preceding inhalation, and finally covers the whole period of exhalation and the respiratory pause. Reciprocity between the inspiratory and expiratory centres is restored. Activity in the accessory muscles gradually fades and dies out.
That the expiratory muscles cease to be involved in the respiratory act earlier during dying and that active exhalation is restored later after resuscitation is evidence that the nerve mechanisms controlling active exhalation are more sensitive to hypoxia than those regulating inhalation.
In most experiments active exhalation developed at the same time as corneal reflexes. A certain relationship between the time of the extinction of corneal reflexes and the exclusion of the expiratory muscles from the respiratory act during dying and the time when the corneal reflexes and active exhalation develop after resuscitation give grounds to suppose that the brain stem formations involved in the development of active exhalation are located on the boundary between the medulla oblongata and the pons varolii.
The second and third types of normalization of the structure of the respiratory act are observed after six to eight minutes of clinical death, cardiac activity being restored during the first four minutes after the beginning of resuscitation, breathing on average after 13 min, and corneal reflexes on average after 38 min.
With type II normalization the expiratory muscles contract at the same time as the inspirators and accessories throughout inhalation during the first or subsequent inhalations. Sixteen minutes after breathing is restored, activity develops in the expiratory muscles at the end of the respiratory pause, and subsequently the same biocurrent dynamics are observed in expiratory muscles as in type I — reciprocity between the inhalation and exhalation centres being restored, and electrical activity in the accessory muscles gradually fading and dying out.
With type III normalization electrical activity develops simultaneously in the inhalatory phase in the inspiratory and accessory muscles, as in type I and II. The expiratory muscles begin to contract much later than the inhalatory, and their electrical activity develops immediately throughout the whole exhalation and the respiratory pause, in contrast to the other two types.
With protracted dying, toward the end of agony and in the initial stages after resuscitation, the fused tetanic contractions of the respiratory muscles break up into a series of clonic discharges, with a rhythm corresponding to that of bursts in the reticular formation of the medulla oblongata. Maintenance of the clonic character of these contractions for more than 20 minutes after clinical death points to severe hypoxic damage to the brain stem.
Types II and III restoration of the structure of the respiratory act have not been observed in any experiments involving relatively short periods of hypoxia. In that connection Type II and III restoration, along with the other symptoms of severe hypoxic damage to the brain, is an unfavourable sign for the prognosis of resuscitation.
Comparison of the efficiency of the external breathing during agony with that in the phase of agonal-type breathing after resuscitation has shown that respiratory volume, and consequently the minute volume of breathing correspond more closely to the structure of the respiratory act than to its pneumographic character. Thus, for example, whereas ventilation is 1.2 litres per minute when the volume of one inspiration at the moments of agony in dying is 240 millilitres, ventilation is 4.4 litres per minute when the volume of an inspiration of the same pneumographic character but another structure of the respiratory act during agonal-type breathing after resuscitation is 880 millilitres.
It should also be noted that normalization of breathing is signalled on the pneumogram much earlier during resuscitation than is normalization of the structure of the respiratory act on the EMG. A gradual increase in ventilation is observed only as electrical activity develops in the expiratory muscles, i.e. after active exhalation has been restored. Studies of the structure of the respiratory act during the restorative period following clinical death have made it possible to establish an objective criterion of complete restoration of external breathing, that is the moment of the exclusion of the accessory muscles from the respiratory act.
With the intention of clarifying the role of the efferent impulses coming along the vagus nerves from the pulmonary receptors in shaping rhythmic activity of the respiratory centre during post-terminal states, the dynamics of the structure of the respiratory act were studied in vagotomized dogs. It was found that the respiratory centre began to react in the restorative period to afferent impulses coming from pulmonary receptors several minutes after breathing had been restored, and that afferent impulses reaching the respiratory centre along the vagus nerves, in other words Hering-Breuer reflexes, were not of vital importance for the development of the first inhalation during the initial stages of reanimation.
Vagotomized animals that had been five minutes in clinical death due to blood loss resumed breathing within the same time as those with intact vagus nerves. These findings coincide with the results of Smirenskaya research. She found that breathing was restored in vagotomized animals that had been clinically dead for five minutes due to blood loss on average after 3 minutes 56 seconds. The resumption of adequate circulation in the region of the medulla oblongata is of much greater importance for restoring the activity of the respiratory centre after clinical death. Evidence of this is the early restoration of spontaneous breathing and of activity of the expiratory respiratory centre after ten minutes of circulatory arrest due to ventricular fibrillation in dogs resuscitated by means of a ‘heart and lungs’ apparatus without artificial respiration.
Whereas, however, the first inhalation is due, in the main, to restoration of adequate circulation in the medulla oblongata, reflex stimulation of the respiratory centre proves to be of great importance in the normalization of breathing. It has been shown that in vagotomized dogs, in early restoration of spontaneous breathing and reciprocity between the inspiratory and expiratory centres, normalization of breathing and of the structure of the respiratory act takes place later than in intact animals.
In order to study the respiratory reflexes that close at the level of spinal cord, experiments involving the registration of electromyograms of the respiratory muscles of spinal animals during resuscitation were carried out. After cutting of the spinal cord at the level of the first cervical vertebra, all the main and accessory respiratory muscles, except those whose motor neurons were located above the transection, showed an absence of phasic activity during reanimation after clinical death, only weak tonic activity being preserved.
During artificial respiration it was necessary to increase respiratory volume two or three times above normal to obtain registration of synchronized bursts in all of the respiratory muscles in response to inflation of the lungs. Reflex contractions of the respiratory muscles in response to inflation of the lungs were only observed on a background of fairly well developed tonic activity. There is thus reason to think that the degree of expression of spinal respiratory reflexes depends on the volume of air insufflated during one inhalation and on the excitability of the motor neurons of the spinal cord.
Rhythmic bursts were registered in the diaphragm muscle of spinal animals on a background of artificial respiration by means of apparatus, independently of the rhythm of the artificial ventilation, which indicated activity of the nucleus of the phrenic nerve. Biocurrent bursts with a frequency of six to nine per minute continued to be registered for 90 to 120 seconds in this muscle, even after a solitary inflation of the lungs on a background of discontinued artificial respiration; and their rhythm did not depend on that of the bursts in the crico-thyroid muscle reflecting activity of the respiratory centre in the medulla oblongata. From this fact it can be suggested that the nucleus of the phrenic nerve during posthypoxic states can not only serve to transmit impulses from the respiratory centre of the medulla oblongata, but can also generate its own rhythmic activity.
The structure of the respiratory act during dying from blood loss and in the restoration period following clinical death after cutting of the brain stem at the boundary between the medulla oblongata and the pons varolii was also studied in acute experiments on dogs. The inspiratory and accessory muscles contracted simultaneously in the inhalation phase during gasping after severing of the brain stem while tonic activity was registered in the expiratory muscles, which was inhibited in the inhalation phase. In medullar animals, as in dogs with intact brain stems, in most cases the expiratory muscles contracted during inhalation simultaneously with the inspiratory and accessory muscles.
In contrast to accepted idea of the identity of gasping after severance of the medulla oblongata from the pons varolii and gasping during agony it has been demonstrated that these two types of respiration have different structures of respiratory act and so consequently different mechanisms. The agonal respiration during dying and in the initial stages after resuscitation of medullar animals does not differ as regards structure from the agonal respiration of dogs with intact brain stems. This leads to the conclusion that agonal respiration is controlled through autonomous mechanisms of the medulla oblongata and is independent of the influence of the higher sectors of the brain. At the same time the gasping centre is highly resistant to hypoxia; medullar animals can maintain agonal respiration for tens of minutes in the presence of extremely low arterial pressure.
The studies of the structure of the respiratory act carried out in our Laboratory gave us a chance not only to understand the mechanisms of extinction and restoration of external breathing during terminal states more deeply, but also to reveal several features of the respiratory centre’s functional organization and rhythmic activity.
Investigation of the electrical activity of the respiratory muscle enables an objective criterion of the full restoration of external breathing in post-terminal state to be established, and also indications for stopping artificial ventilation of the lungs. The increased work of the respiratory muscles calls for extra expenditure of energy, which is particularly undesirable when hypoxia has not been eliminated. Artificial respiration should therefore be discontinued only with full normalization of the structure of the respiratory act, i.e. after electrical activity has disappeared in the accessory respiratory muscles.