Diaphragm and Phrenic Nerve Ultrasound in COVID-19 Patients and Beyond: Imaging Technique, Findings, and Clinical Applications

Abstract

The diaphragm, the principle muscle of inspiration, is an under-recognized contributor to respiratory disease. Dysfunction of the diaphragm can occur secondary to lung disease, prolonged ventilation, phrenic nerve injury, neuromuscular disease, and central nervous system pathology. In light of the global pandemic of coronavirus disease 2019 (COVID-19), there has been growing interest in the utility of ultrasound for evaluation of respiratory symptoms including lung and diaphragm sonography. Diaphragm ultrasound can be utilized to diagnose diaphragm dysfunction, assess severity of dysfunction, and monitor disease progression. This article reviews diaphragm and phrenic nerve ultrasound and describes clinical applications in the context of COVID-19.

Keywords: COVID-19; SARS-CoV-2; diaphragm; phrenic; ultrasound.

© 2021 American Institute of Ultrasound in Medicine.

Figures

Figure 1

Illustration of diaphragm and phrenic nerve anatomy. Original artwork by David C Botos.

Figure 2

Illustration of ultrasound probe positioning for evaluation of the diaphragm utilizing intercostal and subcostal windows. Original artwork by David C Botos.

Figure 3

Normal diaphragm and phrenic nerve ultrasound in a healthy volunteer. A, Illustration depicts diaphragm anatomy as seen on ultrasound with an intercostal window. B, Ultrasound of the right hemidiaphragm utilizing an intercostal window at expiration demonstrates normal muscle size with no evidence of atrophy (thickness >0.15). The diaphragm (calipers) is identified as the muscle between the hyperechoic pleural and peritoneal lines, with a characteristic central tendon slip. C, Ultrasound of the right hemidiaphragm utilizing an intercostal window at inspiration demonstrates intact contractility function with appropriate increase in size of the muscle compared to the expiration image (thickening ratio > 1.2). D, Ultrasound of the right hemidiaphragm utilizing a subcostal window is performed to assess excursion. Cine clips during breathing can demonstrate intact versus decreased motility of the hemidiaphragm. Direct observation by the radiologist is helpful for determining paradoxical movement. Any pertinent findings such as pleural effusion or hepatomegaly should be noted in this view. E, M‐mode ultrasound of the right hemidiaphragm utilizing a subcostal window demonstrates normal excursion. F, Sheer wave elastrography of the hemidiaphragm can be performed utilizing the intercostal probe position, by placing the region of interest (pink oval) within the diaphragm muscle. G, H, Longitudinal and transverse ultrasound of the right phrenic nerve (calipers) in the neck demonstrates normal size and echogenicity of the nerve. I, Color Doppler ultrasound may be useful for differentiating the phrenic nerve from adjacent vessels.

Figure 4

59‐year‐old female with prolonged hospital course for COVID‐19 involving intubation and prone positioning. Her hospital course was complicated by tracheal stenosis status post tracheal resection and anastomosis with multiple subsequent episodes of acute mixed respiratory failure requiring multiple reintubations. Clinical concern was for left hemidiaphragm dysfunction as a contributing factor to her on‐going post‐COVID‐19 respiratory symptoms. A, Ultrasound of the left hemidiaphragm (calipers) on expiration demonstrates normal muscle size (thickness >0.15 cm). B, Ultrasound of the left hemidiaphragm (calipers) on inspiration demonstrates minimal increase in size of the muscle, compatible with poor contractility function (thickening ratio <1.2).

Figure 5

62‐year‐old male with history of HIV and prolonged hospital course for COVID‐19 related ARDS necessitating intubation and prone positioning. He was discharged to an inpatient rehabilitation facility where he was found to have multiple neuropathies confirmed with electromyography and nerve conduction studies. There was clinical concern for phrenic neuropathy potentially contributing to his ongoing post‐COVID‐19 respiratory symptoms. A, B, Ultrasound of the right hemidiaphragm (calipers) on expiration and inspiration views demonstrates normal muscle size (thickness >0.15 cm) with decreased contractility function (thickening ratio <1.2). C, M‐mode ultrasound of the right hemidiaphragm demonstrates decreased excursion with motility elicited only by promoting the patient to breathe deeply. D, The right phrenic nerve (calipers) was normal in size and echogenicity within the neck.

Figure 6

72‐year‐old male with prolonged hospital course for COVID‐19 complicated by invasive pulmonary aspergillosis with multiple post‐COVID‐19 left upper extremity peripheral neuropathies. Clinical concern was for left phrenic neuropathy. Ultrasound of the bilateral hemidiaphragms demonstrated normal muscle size, contractility, and excursion (not shown). A, B, Longitudinal and transverse ultrasound of the left phrenic nerve (calipers) in the neck demonstrates subtle asymmetric thickening and hypoechogenicity. C, D, Normal appearance of the right phrenic nerve (calipers) in the neck on longitudinal and transverse ultrasound is shown for comparison. In the clinical context, findings were affirmative of a left phrenic neuritis diagnosed prior to onset of end‐organ damage (i.e., diaphragm muscle atrophy and dysfunction).

Figure 7

51‐year‐old female with COVID‐19 on mechanical ventilation and ECHMO support transferred from an outside institution for evaluation for potential lung transplantation. A, Chest radiograph demonstrated bilateral infiltrative lung opacities, compatible with known COVID‐19 pneumonia. Elevated right hemidiaphragm was noted, prompting request for diaphragm ultrasound. Portable ultrasound of the diaphragm was performed due to patient's inability to wean from mechanical ventilation for the exam. Respiratory therapist was present during the ultrasound exam and confirmed that the patient's inspiratory effort triggered the ventilator appropriately. B, Ultrasound of the right hemidiaphragm demonstrates normal muscle size (thickness >0.15 cm). C, M‐mode ultrasound of the right hemidiaphragm demonstrates poor excursion with little to no motion detected. Findings are compatible with diaphragm paralysis.

Figure 8

54‐year‐old male with history of COVID‐19 related ARDS status post lung transplantation as a life‐saving intervention of last resort with postoperative course complicated by neuromuscular weakness and hypoventilatory respiratory failure. A, Pre‐transplant chest radiograph demonstrates diffuse lung infiltrates compatible with known COVID‐19 related ARDS. B, Post‐transplant chest radiograph demonstrates elevation of the right hemidiaphragm. C, D, Ultrasound of the right hemidiaphragm (calipers) on expiration and inspiration demonstrates decreased contractility thickening ratio <1.2 with borderline muscular atrophy (thickness = 0.14 cm at end expiration). E, M‐mode ultrasound of the right hemidiaphragm demonstrates poor excursion with little to no motion detected. Findings are compatible with hemidiaphragm paralysis.

Figure 9

64‐year‐old female with history of pulmonary sarcoidosis and idiopathic elevated left hemidiaphragm with acute on chronic respiratory failure in the setting of COVID‐19. A, Chest radiograph demonstrates elevated left hemidiaphragm. B, C, Ultrasound of the left hemidiaphragm (calipers) on expiration and inspiration demonstrates decreased contractility (thickening ratio <1.2) with mild muscular atrophy (thickness = 0.13 cm at end expiration). D, M mode ultrasound of the left hemidiaphragm demonstrates poor excursion with little to no motion detected. E, Ultrasound of the left phrenic nerve (calipers) demonstrates normal size and echogenicity.

Figure 10

Suggested algorithm for clinical use of diaphragm ultrasound. Examples of suspected diaphragm paralysis include elevated hemidiaphragm on chest radiograph or CT, difficulty in weaning from mechanical ventilation, chronic respiratory symptoms following COVID‐19, respiratory symptoms following cardiothoracic surgery or line placement, persistent respiratory symptoms after weaning from mechanical ventilation, and known neuromuscular disorder or chronic lung disease. Diaphragm ultrasound has been proposed as a screening tool in COVID‐19 patients with severe pulmonary involvement to triage and guide management decisions; however, clear guidelines are not available to date and hence have not been put into practice at our institution. Of note, sensitivity and specificity of phrenic nerve sonography is unknown and hence negative imaging does not rule out neuropathy.