Objectives

1. To describe the physiology of the diaphragm muscle.
2. To list the causes of diaphragmatic weakness.
3. To describe the clinical presentation of diaphragmatic paresis and paralysis.
4. To know the diagnostic studies used to confirm diaphragmatic paresis and paralysis.
5. To list the treatment options for diaphragmatic weakness and paralysis.

Key words: diaphragm; paralysis; paresis; phrenic nerve; respiratory failure

Abbreviations
ALS = amyotrophic lateral sclerosis; AP = anterior-posterior; Dlco = diffusing capacity of the lung for carbon monoxide; EMG = electromyography or electromyogram; FRC = functional residual capacity; MIP = maximal inspiratory pressure; Pab = intraabdominal pressure; Pdi = transdiaphragmatic pressure; Pdimax = maximal transdiaphragmatic pressure; Ppl = pleural or intrathoracic pressure; REM = rapid eye movement; TLC = total lung capacity; VA = alveolar volume; VC = vital capacity

Definitions and Introduction

The diaphragm is the principal inspiratory muscle. The diaphragm descends with contraction, which leads to increased thoracic volume, negative intrathoracic pressure, and air entry into the lungs. The diaphragm is responsible for about two thirds of the tidal volume during tidal breathing.¹ Diaphragmatic paresis is characterized by decreased strength of the muscle, while diaphragmatic paralysis is extreme muscle weakness such that no force of contraction is detectable. Diaphragmatic paresis and paralysis may be unilateral or bilateral. Diaphragmatic weakness may be caused by any lesion along the neuromuscular axis, including motor neurons of the spinal cord, the phrenic nerve, the neuromuscular junctions, and of the muscle itself. Unilateral diaphragmatic paresis or paralysis is often asymptomatic. However, bilateral diaphragmatic paralysis can lead to dyspnea on exertion, orthopnea, and even respiratory failure, particularly if other respiratory muscles are weak or if there is an underlying lung disease. Diaphragmatic weakness might be suggested by radiographic findings or the results of pulmonary function tests, but the diagnosis must be confirmed by a fluoroscopic sniff test, measurement of the transdiaphragmatic pressure, or electromyography (EMG) and nerve conduction studies. Treatment options include positive pressure ventilation, phrenic nerve pacing, and diaphragmatic plication.

Physiology and Pathophysiology of the Diaphragm

The diaphragm is the primary muscle responsible for inspiration during relaxed tidal volume breathing. When a person takes a breath, signals from the medulla travel down descending pathways to activate the anterior horn cells of the spinal cord. Nerve roots at C3-C5 form the phrenic nerves, which innervate the diaphragm.

The diaphragm is an elliptical muscle with a central tendon and muscular domes that attach to the inner aspect of the lower ribs, the sternum, and the lumbar vertebrae.² It is innervated by the phrenic nerve, which arises from motor neurons at C3-C5. This muscle contracts during inspiration, moving in a caudal direction, which produces negative pleural and intrathoracic pressure. This negative intrathoracic pressure is transmitted to the alveoli, and as alveolar pressure drops below atmospheric pressure, air is driven from the atmosphere into the lung. If the caudal contraction of the diaphragm were its only action, the negative intrathoracic pressure created would result in inward displacement of the rib cage, which, in turn, would lead to expiration of air from the chest. However, the diaphragm's zone of apposition –the part of the muscle that lies directly against the inner aspect of the lower rib cage–is exposed to positive abdominal pressure, so diaphragmatic contraction leads to expansion of the rib cage. Contraction of the zone of apposition results in outward displacement of the lower rib cage, resulting in chest expansion and negative intrathoracic pressure. Interestingly, in obstructive lung disease, the lungs are hyperinflated, which decreases the size of the zone of apposition. This results in a mechanical disadvantage for inspiration.²

Accessory muscles of inspiration include the intercostal muscles, scalenes, sternocleidomastoids, and trapezii. During tidal volume breathing, the activity of the intercostal muscles serves to stabilize the rib cage. However, all these muscles become active during times of increased ventilation, or to achieve inspiration of tidal volume during diaphragmatic paralysis.

Expiration to functional residual capacity (FRC) normally occurs passively as a result of the inherent recoil of the lung. With ventilatory stress, expiratory muscles actively contribute to expiration. In diaphragmatic paralysis, the expiratory muscles are recruited during expiration, pushing the diaphragm upward into the thorax at end-expiration. Then, during inspiration, there is passive descent of the diaphragm to FRC. In this way, recruitment of expiratory muscles optimizes positioning of the paralyzed diaphragm, preventing paradoxical ascent and net expiratory activity of the diaphragm during inspiration.³

Because the accessory muscles of inspiration and the muscles of expiration largely compensate for the paralyzed diaphragm, isolated diaphragmatic paralysis rarely leads to alveolar hypoventilation and respiratory failure. However, this outcome is much more likely when the underlying disease process also results in generalized neuromuscular weakness.⁴

Etiology of Diaphragmatic Paresis and Paralysis

Diaphragmatic paresis and paralysis may result from a defect at any point along the neuromuscular axis, including the spinal cord, phrenic nerve, neuromuscular junction, and muscle. Cerebrovascular accidents may lead to decreased electrical activity of the diaphragm.^5,6 In one study of 34 patients with acute cerebrovascular accidents, 41% had decreased diaphragmatic excursion. Hemiplegic patients were found to have more hypoxia and hypocapnia.⁷

Spinal cord lesions above the take-off of the phrenic nerve at C3-C5 can lead to diaphragm paralysis. In fact, high spinal cord lesions have severe clinical consequences because most of the accessory muscles of respiration, including the intercostals and abdominal muscles, are paralyzed as well. In these cases, only the sternocleidomastoids and trapezii are intact.⁸ Hypertrophy of the remaining muscles with glossopharyngeal breathing follows in these cases.⁹

The anterior horn cells are the motor neurons of the spinal cord. They receive information from descending pathways. Because anterior horn cells at C3-C5 give rise to the phrenic nerves, motor neuron disease can lead to diaphragmatic weakness. Diseases of the motor neuron include amyotrophic lateral sclerosis (ALS), spinal muscular atrophy, and poliomyelitis.

Because the diaphragm is innervated solely by the phrenic nerves, damage of any type to the latter can lead to diaphragmatic weakness. The phrenic nerves run from the cervical spine in the neck through the mediastinum to the diaphragms. Therefore, they are susceptible to damage from thoracic surgeries or tumors as well as chest trauma. Neuropathies such as Guillain-Barré syndrome and herpes zoster can affect the phrenic nerves, leading to diaphragmatic weakness. Isolated phrenic neuropathies can also be idiopathic. Activation of the diaphragm by the phrenic nerve depends on transmission of the signal across the neuromuscular junction. The machinery that accomplishes this can be impaired by several diseases, including myasthenia gravis, Lambert-Eaton syndrome, and botulism toxicity. The diaphragm muscle itself can be affected by myopathies or metabolic disorders that weaken muscles systemically. Processes that affect the diaphragm itself include muscular dystrophies, thyroid disorders, and polymyositis/dermatomyositis.

The position of the diaphragm at rest or FRC is a function of the inward recoil of the lung and the outward recoil of the chest wall. Disorders of the chest wall and obstructive lung diseases can alter FRC, which affects the length of the diaphragm at rest. The strength of the diaphragm, as with any muscle, depends on its length. Obstructive lung disease involves decreased lung recoil leading to hyperinflation, which places the diaphragm on a suboptimal point on its length-tension curve. Chest wall disorders affect diaphragmatic strength both by altering the length of the diaphragm and by affecting the integrity of the zone of apposition and the way in which the chest wall responds to diaphragmatic contraction.⁹

Clinical Manifestations

Isolated diaphragmatic weakness, without weakness of other muscles of respiration, may have only subtle clinical manifestations.¹⁰ Unilateral diaphragmatic paralysis is often asymptomatic, although some patients have dyspnea on exertion.¹¹ Obviously, unilateral diaphragmatic weakness superimposed on intrinsic lung disease results in worsened symptoms. Physical examination findings may include decreased or paradoxical diaphragmatic excursion, reduced breath sounds at the base of the lung, and asymmetric motion of the abdominal wall.

Bilateral diaphragmatic paralysis presents with dyspnea on exertion and orthopnea. In the upright position, the accessory muscles are able to achieve sufficient minute ventilation in the absence of any diaphragmatic activity, although the diaphragm may be pulled upwards into the thorax to some degree by the negative intrathoracic pressure. However, when the patient reclines and the effect of gravity is removed, the abdominal contents displace the diaphragm into the thorax, leading to low tidal volumes and atelectasis, and hence orthopnea. In addition to the upward displacement of the weak diaphragm during recumbency, the movement of abdominal contents into the thorax expands the rib cage, and places the intercostal muscles at a suboptimal length for contraction, which exacerbates respiratory muscle weakness. In contrast to the orthopnea characteristic of congestive heart failure, the orthopnea of diaphragmatic paralysis occurs immediately after the patient is placed in the supine position. Interestingly, the presence of orthopnea, and not the degree of dyspnea, correlates with diaphragmatic strength.¹ Along the same lines, patients often experience dyspnea when submerged in water (eg, while swimming). The deeper the water into which the erect patient is submerged, the higher the pressure on the abdomen, which leads to inward displacement of the abdominal wall and upward displacement of the diaphragm.^12,13

In bilateral diaphragmatic paralysis, the physical examination can be impressive. There is often rapid, shallow breathing and use of accessory muscles. Dullness to percussion at the lung bases is related to atelectasis due to elevated hemidiaphragms. If assessed through percussion, diaphragmatic excursion will be decreased. Paradoxical inward movement of the abdomen on inspiration, which is particularly evident in the supine position, is highly suggestive of diaphragmatic weakness. In the setting of diaphragmatic paralysis, as the accessory muscles expand the rib case, the negative intrathoracic pressure is transmitted to the abdomen, leading to upward displacement of the paralyzed diaphragm into the thorax and paradoxical, inward movement of the abdominal wall. Severe bilateral diaphragmatic paralysis is usually associated with paradoxical abdominal movement, although patients with milder paresis or unilateral diaphragm paralysis often have normal abdominal movement.¹If paradoxical abdominal movement is not apparent by simple inspection, palpation under the costal margins can evaluate for descent of the diaphragm during inspiration.

With diaphragmatic weakness, but not complete paralysis, the muscle can fatigue. This may lead to a breathing pattern in which the diaphragm and the accessory muscles alternate between abdominal and rib cage breathing (respiratory alternans ).¹⁴

Diaphragmatic Paralysis and Sleep

Early studies revealed alveolar hypoventilation and hypercapnia during sleep as well as symptoms of poor sleep quality, including daytime hypersomnolence and morning headaches, in patients with bilateral diaphragmatic paralysis.⁴ Furthermore, the most profound hypoventilation and hypoxemia have been found to occur during rapid eye movement (REM) sleep.¹⁵ In REM sleep, the voluntary muscles including the accessory muscles of respiration are paralyzed, so breathing becomes dependent on activity of the diaphragm. In normal subjects, tidal volume is largely preserved in REM sleep owing to an increase in diaphragmatic muscle activity,¹⁶ although minute ventilation is slightly decreased due to a decreased respiratory rate. However, in the setting of diaphragmatic paralysis, tidal volume cannot be maintained in REM sleep, which results in hypoventilation and oxygen desaturation.^15,17 In a recent study of patients with ALS, Arnulf and coauthors¹⁸ found that those patients with diaphragmatic weakness had little or no REM sleep. Interestingly, among those ALS patients with diaphragmatic weakness, longer REM duration was associated with preservation of accessory muscle function during REM. There is even some evidence that patients with bilateral diaphragmatic paralysis can maintain a normal quantity of REM sleep through activation of accessory muscles arising from brainstem reorganization.¹⁹ The poor sleep quality observed in patients with diaphragmatic weakness is thought to be due to increasing desaturation at night. Because of the frequent awakenings, diaphragmatic weakness may present clinically with symptoms of poor sleep quality, such as daytime hypersomnolence and morning headaches.

Although diaphragmatic paralysis classically has been associated with nocturnal hypoventilation and hypoxemia,^4,15,20 recent studies have had conflicting results. In one study of six patients with isolated bilateral diaphragmatic paralysis in the absence of generalized neuromuscular weakness, only two showed significant oxygen desaturation, and Pco₂ levels remained within normal limits in all patients. In addition, the number of arousals was normal and there were no detectable symptoms of poor sleep quality.¹⁰ The authors conclude that nocturnal hypoventilation requires generalized neuromuscular weakness rather than isolated diaphragmatic paralysis. In fact, some reports suggest that even patients with generalized neuromuscular disease who have fragmented sleep, particularly in the REM phase, may not demonstrate the profound nocturnal hypoventilation and desaturation that is classically associated with diaphragmatic weakness.¹⁸ However, the data are conflicting, as some patients with even isolated diaphragmatic paralysis demonstrate severe oxygen desaturation during REM sleep.²¹ Full polysomnography should be part of the routine workup of patients with diaphragmatic dysfunction.

Diagnosis

While the chest radiograph, pulmonary function testing, and arterial blood gas analysis can suggest diaphragmatic weakness, the conclusive diagnosis is usually made by a fluoroscopic sniff test, transdiaphragmatic pressure measurements, a phrenic nerve conduction study, and/or diaphragm EMG.

Resting arterial blood gas is usually normal in unilateral diaphragmatic paralysis. In bilateral diaphragmatic paralysis, the Po₂ may be normal or may be decreased as a result of shunting of blood past atelectatic lung. Likewise, the Pco₂ may be normal, decreased, or increased. Often, the atelectasis and hypoxemia that result from diaphragmatic paralysis lead to increased minute ventilation and a fall in Pco₂ . However, in some patients, diaphragmatic paralysis results in decreased tidal volumes, alveolar hypoventilation, and therefore increased Pco₂. Hypercapnia usually occurs when overall respiratory muscle strength [maximal inspiratory pressure (MIP)] is <30% predicted and when vital capacity (VC) falls to <55% of predicted.²² Supine arterial blood gases are more sensitive for diaphragmatic paralysis. A fall in Pco₂ by 5 to 25 mmg Hg and a rise in Pco₂ by an average of 5 mm Hg can be expected when the patient lies supine.⁴

With significant diaphragmatic weakness, pulmonary function test findings are characterized by a restrictive pattern and decreased diffusing capacity of the lung for carbon monoxide (Dlco) but normal Dlco/alveolar volume (AV). In one study of patients with isolated diaphragm weakness, the average total lung capacity (TLC) was 67±11% predicted and D lco was 65±12% predicted with a normal or increased Dlco/AV.¹⁰ VC is often used as a predictor of hypercapnic respiratory failure due to neuromuscular disease, but it is an insensitive measure of lesser degrees of diaphragmatic weakness, in addition to being nonspecific. In unilateral diaphragmatic paralysis, VC in the upright position is usually around 75% of predicted and decreases by 15 to 25% with supine positioning. The effect of supine positioning on the VC is greater when the right hemidiaphragm is paralyzed, as a result of displacement of the liver into the chest.^23,24 With bilateral diaphragmatic paralysis, VC can be reduced to <50% of predicted.⁹ However, seated VC is an insensitive measure of diaphragmatic weakness and doesn't fall until weakness becomes significant. Upright VC only weakly correlates with measurements of diaphragmatic strength. This is because the shape of the pressure-volume curve flattens at both low and high volumes, so that moderate degrees of weakness only have a small effect on lung volumes.¹ If there is significant weakness, a fall in lung volumes will be seen. With supine positioning, there is a further decrease in VC. The normal fall in VC with supine positioning is <20%; in patients with obstructive lung disease, it can be somewhat higher. A fall in VC >25% with normal lung function or >35% associated with obstructive lung disease should raise suspicion for diaphragmatic weakness. 25 In patients with bilateral diaphragmatic paralysis, the vital capacity may fall by up to 50% when they are supine.^1,4 Unlike the upright VC, the supine fall in VC has been shown to correlate with direct measurements of diaphragmatic strength.¹

In addition to VC, MIP is often used to assess patients for diaphragmatic weakness. In fact, the MIP has been shown to correlate with transdiaphragmatic pressure, the gold standard for the measurement of diaphragmatic weakness.¹ However, this is highly nonspecific because it is an effort-dependent maneuver. Furthermore, the sensitivity of the MIP is limited by the fact that the compensatory actions of the accessory muscles can achieve a normal MIP. MIP reflects global inspiratory strength rather than isolated diaphragmatic function. Maximal expiratory force is usually normal in diaphragmatic paralysis, as expiration is achieved primarily by accessory muscles without contribution from the diaphragm. The 12-s maximum voluntary ventilation can also be low, and has been shown to correlate with transdiaphragmatic pressure.¹⁰

The chest radiograph classically reveals elevated hemidiaphragms or low lung volumes in diaphragmatic weakness, but these are neither sensitive nor specific. In bilateral diaphragmatic paralysis, the symmetric elevation of both hemidiaphragms, often with subsegmental atelectasis at the bases of the lungs, is easily interpreted as low lung volumes.

Fluoroscopy is commonly used to assess for diaphragmatic weakness. Classically, paradoxical upward movement of diaphragm is seen during sniff inspiration. A threshold of 2 cm is often used because normal subjects may have paradoxical upward movement of the diaphragm during inspiration up to 2 cm. The sniff test is much more sensitive for the diagnosis of unilateral diaphragmatic paralysis, in which paradoxical elevation of the affected hemidiaphragm with inspiration is seen in >90% of patients.²⁶ In bilateral diaphragm paralysis, the abdominal muscles can contract during expiration, pushing the diaphragm up. Then, during inspiration, the diaphragm can passively descend to a resting position, leading to a false-negative sniff test. In addition, when the accessory muscles achieve upward movement of the thoracic cage during inspiration, there can appear to be a relative downward displacement of the diaphragm.²⁷ Finally, the test can give false-negative results if it is not performed in the supine position, which can be difficult for patients with true diaphragmatic paralysis.

Historically, measurement of chest and abdominal dimensions were done during respiratory cycle to assess for paradoxical movement. This is known as the Konna and Mead model. The anterior-posterior (AP) diameter of the rib cage and the abdominal wall can be measured by placing magnetometers on the body surface. Magnetometer coils are attached at the level of the fifth intercostal space to measure the rib cage AP diameter. Another magnetometer is attached 2 cm above the umbilicus to measure the abdominal AP diameter. Expansion of the rib cage and abdominal wall can be measured during quiet tidal breathing or during inspirations to TLC, both in the upright and supine positions.¹ A normal breathing pattern is characterized by an increase in the AP diameter of both the rib cage and abdomen during inspiration. In diaphragmatic weakness, the abdomen is pulled inward due to expansion of the thorax and passive upward displacement of the weak diaphragm.²⁷

The gold standard for the diagnosis of diaphragamatic weakness is the maximal transdiaphragmatic pressure (Pdimax). While MIP assesses global inspiratory muscle activity, Pdimax specifically assesses the strength of the diaphragm. A nasogastric catheter is inserted with one balloon pressure sensor in the esophagus and one in the stomach. Esophageal pressure estimates pleural or intrathoracic pressure (Ppl), and gastric pressure represents intraabdominal pressure (Pab). Then, Pdi = Pab - Ppl.

• At FRC, transdiaphragmatic pressure (Pdi) is zero.
• With an intact diaphragm muscle, which descends during inspiration, Pab increases and Ppl decreases during inspiration. Therefore, Pdi is positive. A normal Pdi is >25 cm H₂O.
• In diaphragmatic paralysis, the negative intrathoracic pressure generated by the accessory muscles is transmitted across a flaccid diaphragm, because the thorax and abdomen effectively act as one compartment. In this case, Ppl = Pab, and Pdi is zero.
• In diaphragm weakness, rather than complete paralysis, Pdi is reduced but greater than zero.
• A decline in Pdimax over a short period of time (eg, hours) suggests diaphragmatic fatigue.

Pdi can be measured during slow inspirations to TLC, maximal static inspiratory efforts, and a maximal sniff maneuver. Sniff Pdi produces the maximal and most reproducible values.¹ Maximal and reproducible values of the Pdi measurement are achieved by the visual feedback technique, in which the subject watches Ppl and Pab fluctuate on a monitor. Transdiaphragmatic pressure can also be measured after electrical stimulation of the phrenic nerve in the neck, a measurement that is independent of effort.²⁸ Pdi has been shown to correlate with the level of dyspnea, orthopnea, abdominal paradox, and fall in vital capacity with supine positioning. One study derived an equation to predict Pdi (in cm H₂O) on the basis of noninvasive tests of diaphragmatic strength¹:

Pdi = 36.1 - [0.828(supine fall VC)] + [0.634(Pimax)]

where Pimax is maximal static inspiratory mouth pressure (correlation, 0.80; p<0.0001). Pdi is reduced in some patients with unilateral diaphragmatic paralysis^20,23 and should be highly sensitive for bilateral diaphragmatic paralysis.

EMG can be used to conclusively diagnose complete diaphragmatic paralysis. An EMG can be done during tidal breathing, during maximal inspiratory maneuvers, and after phrenic nerve stimulation. The phrenic nerve is stimulated by percutaneous electrodes in the neck, where the nerve lies in a relatively superficial position just under the sternocleidomastoid. The muscle activity is then measured with surface electrodes placed over the lower rib cage, where the diaphragm contacts the inner ribs. A negative EMG signal confirms diaphragm paralysis. Esophageal electrodes may also be used to measure action potentials in the crural diaphragms without any effect of the intercostal and abdominal muscles. True diaphragmatic paralysis is diagnosed if phrenic nerve stimulation does not result in a diaphragmatic action potential. Of course, decreased action potential of the diaphragm after stimulation of the phrenic nerve is not specific for phrenic neuropathies: myopathies and disorders of the neuromuscular junction will give similar results. However, the EMG pattern and the nerve conduction time distinguish neuropathic from myopathic causes of diaphragmatic paralysis. Nerve conduction time -the time from the nerve stimulation to the EMG potential- can help with the diagnosis of phrenic neuropathies.²⁹ If an action potential is present, Pdi can be measured after phrenic nerve stimulation to assess the mechanical response of the muscle to a successfully transmitted impulse.^28-30

In disease processes with generalized weakness, the diagnosis may be made by EMG or muscle biopsy of muscles that are more easily accessible than the diaphragm. For example, diseases of the anterior horn cells, neuromuscular junction, and muscle itself affect strength outside of the diaphragm, and the diagnosis can be made by EMG or biopsy of more easily affected muscles. Also, blood tests such as thyroid-stimulating hormone, cortisol, electrolytes, creatine kinase, and rheumatologic serologies can be useful.

Similar to plain film, the chest CT usually reveals small lung volumes and basilar atelectasis. Alternatively, myelography may be helpful in the diagnosis of spinal cord lesions. Additional testing that may be performed to workup the etiology of diaphragmatic paralysis includes cervical spine MRI. A sleep study is helpful to assess for worsening hypoxemia arising from atelectasis and hypoventilation in the supine position, as a positive study would alter treatment.

Treatment

In rare cases, diaphragmatic paralysis is reversible, but in most cases it is not. There are several options for the treatment of diaphragmatic weakness, and the treatment of choice depends on the severity and the etiology. For patients with daytime and/or nocturnal hypoventilation, noninvasive positive pressure ventilation may be used at night. In one study of patients with neuromuscular disease, symptoms of poor sleep quality, such as headache, daytime fatigue, and cognitive impairment, are improved by the use of nocturnal continuous positive airway pressure. In addition, in this study, daytime arterial Po₂ and Pco₂ improved with therapy.³¹ In another study, transdiaphragmatic pressures improved after a period of ventilatory support.³² Permanent positive pressure ventilation via tracheostomy is used for high cervical spine injuries.

Diaphragmatic pacing is another option for the treatment of diaphragmatic paralysis. In cervical spinal cord lesions above C3, the C3-C5 motor neurons and the phrenic nerve remain intact. Therefore, phrenic nerve pacing is a feasible treatment option. Before placement of the device, an EMG should be performed to ensure that the phrenic nerve is functionally intact. The pacer is then implanted into the phrenic nerves in the neck or the chest and controlled by a stimulating unit that is external to the body. There is a conditioning period, during which the diaphragm regains function after its period of paralysis, and this may be complicated by hypercapnia. If successful, diaphragmatic pacing may provide normal pulmonary function and arterial blood gases as well as a decreased incidence of respiratory infections. Theoretical concerns about nerve damage resulting from pacing have not been borne out in the literature.³³ In spinal cord lesions affecting the C3-C5 motor neurons, the efficacy of diaphragmatic pacing depends on the level of the lesion. Unfortunately, when these motor neurons are damaged, the phrenic nerve is damaged, and denervation leads to atrophy of the diaphragm muscle.

Unilateral diaphragmatic paralysis is usually asymptomatic, but when it produces symptoms in the setting of strenuous exertion or underlying lung disease, it may be treated. Diaphragmatic plication has been shown to result in improvements in oxygenation and lung volumes as well as symptoms, and is associated with little morbidity.^34,35 The procedure prevents the paralyzed diaphragm from being pulled up into the thorax by the negative pressure generated by the healthy diaphragm. This improves ventilation to the ipsilateral lung and reduces the workload of the contralateral diaphragm, preventing fatigue.

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