- Open Access
The role of spontaneous effort during mechanical ventilation: normal lung versus injured lung
© Yoshida et al.; licensee BioMed Central. 2015
- Received: 16 January 2015
- Accepted: 12 March 2015
- Published: 17 June 2015
The role of preserving spontaneous effort during mechanical ventilation and its interaction with mechanical ventilation have been actively investigated for several decades. Inspiratory muscle activities can lower the pleural components surrounding the lung, leading to an increase in transpulmonary pressure when spontaneous breathing effort is preserved during mechanical ventilation. Thus, increased transpulmonary pressure provides various benefits for gas exchange, ventilation pattern, and lung aeration. However, it is important to note that these beneficial effects of preserved spontaneous effort have been demonstrated only when spontaneous effort is modest and lung injury is less severe. Recent studies have revealed the ‘dark side’ of spontaneous effort during mechanical ventilation, especially in severe lung injury. The ‘dark side’ refers to uncontrollable transpulmonary pressure due to combined high inspiratory pressure with excessive spontaneous effort and the injurious lung inflation pattern of Pendelluft (i.e., the translocation of air from nondependent lung regions to dependent lung regions). Thus, during the early stages of severe ARDS, the strict control of transpulmonary pressure and prevention of Pendelluft should be achieved with the short-term use of muscle paralysis. When there is preserved spontaneous effort in ARDS, spontaneous effort should be maintained at a modest level, as the transpulmonary pressure and the effect size of Pendelluft depend on the intensity of the spontaneous effort.
- Spontaneous breathing
- Muscle paralysis
- Lung injury
- Pleural pressure
- Transpulmonary pressure
The role of spontaneous breathing during mechanical ventilation has been discussed for several decades [1-4]. From a physiological point of view, spontaneous breathing during mechanical ventilation provides various beneficial effects, including the maintenance of the end-expiratory lung volume, predominant dorsal ventilation, better gas exchange, and prevention of diaphragmatic dysfunction [1-9]. Thus, spontaneous effort has traditionally been encouraged to be preserved during mechanical ventilation [1,2]. Recent experimental studies, however, have shed light on the negative impacts of spontaneous breathing, especially in severe forms of ARDS [10-12]. Further, recent clinical studies have revealed the beneficial impacts of eliminating all muscle activities by neuromuscular blocking agents in severe forms of ARDS [13-16]. These different impacts of spontaneous breathing during mechanical ventilation may be explained by different inflation patterns that are observed in normal (fluid-like) lungs versus injured (solid-like) lungs and transpulmonary pressure. The goals of this review are to summarize the physiological mechanisms of different lung ventilation in normal lungs versus injured lungs, raise important concerns about spontaneous breathing in ARDS, and present an updated discussion on the role of spontaneous breathing and muscle paralysis during mechanical ventilation in ARDS.
Mechanism to determine the diaphragmatic force
As the main inspiratory muscle, the diaphragm contributes 72% of tidal breath, and its role in respiratory mechanics and gas exchange is also very significant . When spontaneous effort starts, diaphragmatic fibers develop tension and shorten. As a result, the dome of the diaphragm, which essentially corresponds to the central tendon, descends relative to the costal insertions of the muscle, resulting in two main effects . First, it expands the thoracic cavity along its craniocaudal axis. Accordingly, pleural pressure (P pl) falls and lung volume increases. Second, it produces a caudal displacement of the abdominal viscera and an increase in abdominal pressure, which, in turn, pushes the ventral abdominal wall outward . This pressure-generating capacity of the diaphragm is traditionally accepted to be determined by several factors, but the force-length relationship of the diaphragm and its radius of curvature are the most significant.
The force-length relationship of the diaphragm
In dogs, cats, rabbits, and humans, the negative swings in P pl with phrenic nerve stimulation have been proven to decrease with increasing end-expiratory lung volume before starting phrenic nerve stimulation [19-22]. As a typical example, Pengelly et al. reported that in cats, the negative swings in P pl with phrenic nerve stimulation decreased rapidly and continuously from −13 cm H2O to −8.5 (or −10.5) cm H2O when inflated with a volume of 20 (or 10) ml from functional residual capacity . Thus, the pressure-generating capacity of the diaphragm decreases when the end-expiratory lung volume increases. This observation is explained by the mechanism known as the force-length relationship of the diaphragm, which is the idea that the isometric force developed by a muscle decreases when its length decreases [19,22-24]. As the length of the muscle bundle increases, the active force gradually increases until a maximum is reached, and it then decreases again. The length corresponding to the maximum active force is usually referred to as the optimal length and is typically achieved at functional respiratory capacity . When the lung volume in animals and humans is increased from residual volume to total lung capacity, the diaphragmatic fibers shorten by 30–40%.
The radius of curvature of the diaphragm
The diaphragm is a curved surface, so the pressure difference across it is proportional to the muscle tension and inversely proportional to the radius of curvature of the muscle (Laplace’s law). As the shape of the diaphragm becomes flatter, the mechanical advantage of converting force into pressure diminishes . Thus, the pressure-generating capacity of the diaphragm is theoretically diminished by increasing the radius of its curvature [20,22,23]. However, in humans, as well as in dogs, the radius of the diaphragm curvature during spontaneous effort remains mostly constant or changes little, independent of the end-expiratory lung volume . At an extreme condition (i.e., phrenic nerve stimulation), the radius of the diaphragm curvature increases sharply . Thus, the pressure-generating capacity of the diaphragm is primarily determined by its force-length relationship, and the shape of the diaphragm is only important during extreme muscle shortening .
Interaction of inspiratory muscles and mechanical ventilation
where transpulmonary pressure is the pressure needed to inflate the lung, airway pressure is the pressure applied by positive-pressure ventilation via the trachea, and pleural pressure is the lung surface pressure imposed by the chest wall.
Ventilation pattern with preserved spontaneous effort in a normal lung
Ventilation pattern with preserved spontaneous effort in injured lungs
It is important to note that the pattern of lung inflation is different in the presence of lung injury. In the injured lung, Pendelluft occurs as a result of the development of a more negative swing in P pl in the dependent lung than in the nondependent lung. Atelectatic tissue may behave less like a fluid and more like a frame of ‘solid’ areas resisting to shape deformation. In this setting, part of the mechanical energy generated by the inspiratory muscle contractions would be exerted on local lung deformation rather than being transmitted to the rest of the lung, thus resulting in imperfect elastic anisotropic inflation .
Inspiratory P L and the effect size of Pendelluft become larger as spontaneous effort increases in strength during mechanical ventilation (Figure 2 and ref. ). Thus, mild spontaneous effort may be beneficial to recruit the collapsed lung, while excessive spontaneous effort could cause local overstretch due to injuriously high P L and the large effect size of Pendelluft [12,36].
Controversial effects of spontaneous breathing in ARDS
The role of spontaneous breathing in mild-moderate ARDS
Thus, it is important to emphasize that it is necessary to avoid strong spontaneous efforts (i.e., not high ∆pleural pressure) and maintain relatively low plateau pressure (i.e., not high ∆airway pressure) in order to prevent the large effect of Pendelluft and injuriously high P L.
The role of spontaneous breathing in severe ARDS
In severe ARDS, however, spontaneous effort during mechanical ventilation is difficult to control and becomes unfavorable . Several plausible explanations can be offered. First, the increases in P L are expected to be greatest in more severe ARDS because in such cases, higher plateau pressure is required from the ventilator, reflecting an impaired respiratory system compliance. In addition, greater diaphragmatic force is often generated by the patient, reflecting the high levels of dyspnea . Injuriously high P L proved to worsen histological lung injury in our previous animal studies [10,11]. Second, we recently revealed an injurious ventilation pattern caused by strong spontaneous effort, i.e., Pendelluft, which is the displacement of gas from nondependent (more recruited) lung to dependent (less recruited) lung during early inspiration . Despite the limitation of tidal volume to less than 6 mL/kg, strong diaphragmatic contraction resulted in unsuspected local overstretch of the dependent lung due to the large effect of Pendelluft, leading to tidal recruitment in dynamic CT acquisitions. Matching this degree of regional overstretch during neuromuscular paralysis required an overall tidal volume of 15 mL/kg (i.e., a highly injurious lung stretch) . Importantly, this injurious ventilation pattern cannot be suspected by using conventional monitoring, such as airway pressure monitoring, flow monitoring, and even esophageal pressure monitoring. Thus, a lung-protective ventilation strategy (i.e., the limitation of plateau pressure and tidal volume) is not effective for reducing the risk of ventilator-induced lung injury unless spontaneous breathing effort during mechanical ventilation is carefully controlled at a modest level.
We often find that the demands of spontaneous breathing effort in severe ARDS is much higher than in less severe ARDS, and as a result, it is quite difficult to control the intensity of spontaneous effort by sedatives . This is likely due to metabolic/respiratory acidosis, hypercapnia, or decreased end-expiratory lung volume due to a large amount of collapsed tissues (mentioned above). So far, the most effective, established strategy is to eliminate spontaneous effort completely by the initiation of neuromuscular blocking agents [13-15]. In the ACURASYS study, the placebo group (i.e., no neuromuscular blockade use) had a higher incidence of barotrauma, even at the comparable plateau pressure and tidal volume, to the muscle paralysis group , suggesting spontaneous effort may have generated injuriously high P L and unsuspected local overstretch of dependent lung regions, which is associated with Pendelluft. However, another simple, safe strategy to reduce the intensity of spontaneous effort needs to be promptly established. As indicated above, the negative swings in P pl generated by diaphragmatic contraction is proven to decrease linearly with increasing end-expiratory lung volume and radius of curvature [19-22]. Considering the mechanical property of the diaphragm to generate the pressure, optimized PEEP with lung recruitment might be effective for reducing the intensity of spontaneous effort by restoring the end-expiratory lung volume and reducing the diaphragmatic radius of curvature. Indeed, previous studies support this aspect because spontaneous breathing effort is typically weaker on high PEEP level than that on low PEEP level during BIPAP [40,41]. This aspect should be explored in future studies.
It is important to balance muscle paralysis versus spontaneous breathing during mechanical ventilation in ARDS, depending on the severity of ARDS, the timing of ARDS, and the ventilatory demands. In the early stage of severe ARDS, partial ventilatory support to promote spontaneous breathing should be avoided, and muscle paralysis may be effective to strictly control P L within the safe range, thus preventing Pendelluft. In less severe forms of ARDS and after the short-term use of muscle paralysis in severe ARDS, spontaneous breathing should be facilitated using partial ventilatory support while avoiding strong spontaneous effort and high plateau pressure.
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