Diaphragm sniff ultrasound: Normal values, relationship with sniff nasal pressure and accuracy for predicting respiratory involvement in patients with neuromuscular disorders

Abstract

Background: In patients with neuromuscular disorders, assessment of respiratory function relies on forced vital capacity (FVC) measurements. Providing complementary respiratory outcomes may be useful for clinical trials. Diaphragm sniff ultrasound (US) is a noninvasive technique that can assess diaphragm function that may be affected in patients with neuromuscular disorders.

Purpose: We aimed to provide normal values of sniff diaphragm ultrasound, to assess the relationship between sniff diaphragm US, vital capacity (VC) and sniff nasal pressure. Additionally, we aimed to evaluate the diagnostic accuracy of sniff diaphragm US for predicting restrictive pulmonary insufficiency.

Materials and methods: We included patients with neuromuscular disorders that had been tested with a sniff diaphragm US and functional respiratory tests. Healthy subjects were also included to obtain normal diaphragm sniff ultrasound. We performed diaphragm tissue Doppler imaging (TDI) and time movement (TM) diaphragm echography combined with sniff maneuver.

Results: A total of 89 patients with neuromuscular diseases and 27 healthy subjects were included in our study. In patients, the median age was 32 years [25; 50] and the median FVC was 34% of predicted [18; 55]. Sniff diaphragm motion using TM ultrasound was significantly associated with sniff nasal pressure, both for the right hemidiaphragm (r = 0.6 p <0.0001) and the left hemidiaphragm (r = 0.63 p = 0.0008). Right sniff peak TDI velocity was also significantly associated with FVC (r = 0.72, p<0.0001) and with sniff nasal pressure (r = 0.66 p<0.0001). Sniff diaphragm ultrasound using either TM mode or TDI displayed significant accuracy for predicting FVC<60% with an area under curve (AUC) reaching 0.93 (p<0.0001) for the right sniff diaphragm ultrasound in TM mode and 0.86 (p<0.001) for right peak diaphragm TDI velocity.

Conclusion: Sniff diaphragm TM and TDI measures were significantly associated with sniff nasal pressure. Sniff diaphragm TM and TDI had a high level of accuracy to reveal respiratory involvement in patients with neuromuscular disorders. This technique is useful to assess and follow up diaphragm function in patients with neuromuscular disorders. It may be used as a respiratory outcome for clinical trials.

Fig 1. Diaphragm ultrasound displacement from the subcostal view in a control subject and in a DMD patient.

Normal right diaphragm sniff time movement (TM) motion in the control group (left); note the sharp upstroke during a sniff maneuver. Pathological right diaphragm motion during a sniff maneuver in a DMD patient (right). Note the reduced diaphragm motion with the sniff maneuver. DMD: Duchenne muscular dystrophy.

Fig 2. Sniff right hemidiaphragm tissue Doppler imaging peak velocity (arrow) in a volunteer (peak velocity = 12 cm/s).

Fig 3. Pathological right hemidiaphragm peak tissue Doppler imaging velocity during a sniff maneuver in a DMD patient.

Note the reduced peak sniff diaphragm TDI velocity (arrow).

Fig 4

Relationship between right diaphragm sniff TM motion and sniff nasal pressure in patients (A), and the relationship between left diaphragm sniff TM motion and sniff nasal pressure in patients (B). TM = time movement; Sniff TM mode = Sniff TM motion.

Fig 5. Relationship between right diaphragm sniff peak TDI velocity and sniff nasal pressure in patients.

Sniff TDI peak inspi = sniff peak diaphragm tissue Doppler imaging velocity.

Fig 6. Relationship between right sniff TM mode and FVC in patients.

FVC: forced vital capacity (%).

Fig 7. Relationship between left sniff TM mode and FVC in patients.

FVC: forced vital capacity (%).

Fig 8. Relationship between right sniff TM mode and FVC (ml) in patients.

FVC: forced vital capacity.

Fig 9. Relationship between right sniff TDI peak velocity (cm/s) and FVC in patients.

FVC = forced vital capacity (%).

Fig 10. Relationship between right sniff diaphragm TM motion and FVC in DMD.

DM1 and other myopathies. DMD = Duchenne muscular dystrophy; DM1 = myotonic dystrophy type I; others = other myopathies; FVC = forced vital capacity (%); sniff M mode = right sniff diaphragm time movement motion (mm).

Fig 11. ROC (receiver operating characteristic) curves for predicting a FVC<60% in patients with neuromuscular disorders.

TDI right: peak sniff TDI velocity (cm/s) at the right hemidiaphragm; M mode left: left diaphragm motion during a sniff maneuver (mm); M mode right: right diaphragm motion during a sniff maneuver (mm); FVC = forced vital capacity (%).

Fig 12. ROC curves for predicting a FVC <30% in patients with neuromuscular disorders.

M mode right: right diaphragm motion during a sniff maneuver; M mode left: left diaphragm motion during sniff maneuver (mm); TDI right: peak sniff TDI velocity (cm/s) recorded at the right hemidiaphragm; FVC: forced vital capacity (%).