Diaphragm thickness and function can be assessed in healthy individuals and critically ill patients using point-of-care ultrasound. This technique offers an accurate, reproducible, feasible, and well-tolerated method for evaluating diaphragm structure and function.
The diaphragm is the main component of the respiratory muscle pump. Diaphragm dysfunction can cause dyspnea and exercise intolerance, and predisposes affected individuals to respiratory failure. In mechanically ventilated patients, the diaphragm is susceptible to atrophy and dysfunction through disuse and other mechanisms. This contributes to failure to wean and poor long-term clinical outcomes. Point-of-care ultrasound provides a valid and reproducible method for evaluating diaphragm thickness and contractile activity (thickening fraction during inspiration) that can be readily employed by clinicians and researchers alike. This article presents best practices for measuring diaphragm thickness and quantifying diaphragm thickening during tidal breathing or maximal inspiration. Once mastered, this technique can be used to diagnose and prognosticate diaphragm dysfunction, and guide and monitor response to treatment over time in both healthy individuals and acute or chronically ill patients.
Ultrasound refers to sound waves beyond the upper audible limits of human hearing. Ultrasound has many applications beyond healthcare, the most famous likely being the development of SONAR (sound navigation and ranging) for military use in World War I1; ultrasound is now routinely used in medical diagnosis and therapy. Medical sonography or diagnostic ultrasound utilizes high frequency sound waves (>20 kHz) to provide images of soft tissue structures within the body. These sound waves are pulsed at frequencies of 1 to 20 million cycles/s (megahertz, MHz), which can be transmitted into the body to examine anatomical structures, such as the liver, heart, and skeletal muscle. Point-of-care ultrasound is increasingly becoming a cornerstone of the evaluation and management of critical illness.
The first application of ultrasound in medicine was in the 1940's by Dr. Karl Dussik, who attempted to locate brain tumors by measuring the transmission of ultrasound beams through the head2. As technology progressed, new techniques were developed, including amplitude mode (A-mode) and brightness mode (B-mode)3, followed by the development of two-dimensional scanners in 19604,5. The field of diagnostic ultrasound has become invaluable in clinical practice, since it avoids exposure to ionizing radiation and can be obtained at the bedside, avoiding the need for in-hospital transport with associated risks. Ultrasound is safe, well-tolerated, reliable, and repeatable in patients6,7.
The diaphragm is a thin, dome-shaped muscular structure that acts as the main respiratory pump driving spontaneous ventilation in humans. The diaphragm separates the thoracic and abdominal cavities and is composed of three separate segments: the central tendon, the costal diaphragm, and the crural diaphragm (Figure 1). The central tendon of the diaphragm is a noncontractile structure that allows major bloods vessels to pass through from the thoracic to the abdominal cavity. The costal diaphragm has fibers running from the rib cage or xiphoid process to the central tendon. The crural diaphragm inserts into the first three lumbar vertebrate. During inspiration, the costal diaphragm contracts, lowering the dome of the diaphragm while expanding the lower rib cage. The costal diaphragm supports the crural diaphragm in the lowering the dome8,9,10.
Transthoracic ultrasound of the diaphragm has gained increasing attention for its ability to monitor diaphragm thickness at the zone of apposition (Figure 1)11,12,13. The diaphragm was first visualized with ultrasound in 1975 by Haber et al.14. Diaphragm contractility and muscular shortening during inspiration can be quantified using M-mode ultrasound to monitor the diaphragm thickness (Tdi) and thickening fraction (TFdi). This assessment of contractility provides a measure of diaphragm muscular performance under a given level of inspiratory drive and effort. Point-of-care ultrasound provides safe, repeatable, and reliable measures of diaphragm function and architecture. In mechanically ventilated patients, changes in diaphragm thickness over time can be used to evaluate the negative impacts of mechanical ventilation, including the effects of myotrauma due to over-assistance (atrophy; decreasing end-expiratory thickness over time) or under-assistance (load-induced injury resulting in inflammation, edema; possibly represented by increasing end-expiratory thickness over time)15. These changes are correlated with adverse clinical outcomes16. Measuring TFdi during tidal breathing permits an assessment of tidal diaphragmatic activity (i.e., inspiratory effort). Measuring TFdi during a maximal inspiratory effort (TFdi,max) provides an assessment of diaphragm strength (since the diaphragm's force-generating capacity is related to its ability to contract and shorten).
There is substantial consensus on the optimal protocol for acquiring and analyzing measurements17. Competency in diaphragm ultrasound imaging involves a moderately steep learning curve; thorough training in the technique and its potential pitfalls is essential. Studies have shown that proficiency in diaphragm ultrasound expertise can be acquired in a short period of time through remote, web-based training18. Therefore, this protocol has been optimized to provide a consistent measurement of diaphragm thickness and thickening fraction that can be applied to both healthy and patients with suspected respiratory pathology19
Studies employing this technique have received ethical approval from the Research Ethics Board at the University Health Network, Toronto, Canada.
1. Evaluating diaphragm thickness and thickening fraction during tidal breathing
Figure 1: Overview of diaphragm anatomy and placement of ultrasound probe. (A) Anatomical structures for ultrasound of the costal diaphragm. The diaphragm consists of the central tendon, costal diaphragm, and crural diaphragm. (B,C) To visualize the the costal diaphragm at the zone of apposition on ultrasound, the patient is placed in the semirecumbent position and the eighth, ninth, or 10th intercostal space is located. A high frequency (>12 MHz) linear array ultrasound probe is placed parallel to the ribs in the intercostal space along the midaxillary line to visualize the costal diaphragm as a cross-section. Please click here to view a larger version of this figure.
Figure 2: Ultrasound diaphragm thickness and thickening during tidal breathing. (A) The probe is placed at the eighth, ninth, or 10th intercostal space to visualize the diaphragm as a cross-section. (B) In the B-mode image, the white arrows demonstrate the hyperechoic pleural and peritoneal membranes. (C) The M-mode image projects variation in diaphragm thickness at a particular point over time. From left to right, the yellow lines measure diaphragm thickness at end expiration (Tdi,ee) and diaphragm thickness at peak inspiration (Tdi,pi) of the first breath, and red lines denote that of the second breath. Diaphragm thickness (Tdi,ee) measures 1.20 and 1.25 mm, and TFdi 26% and 23%, respectively, in a healthy male subject. Please click here to view a larger version of this figure.
Table 1: Common issues in transdiaphragmatic ultrasonography Please click here to download this Table.
2. Evaluating the maximal diaphragm thickening fraction
NOTE: The maximal diaphragm thickening fraction may be assessed during the same experimental session as diaphragm thickness.
Figure 3: Examples of minimal and maximal diaphragm thickening fraction. (A) Ultrasound diaphragm thickness (Tdi) and thickening fraction (TFdi) were measured in the presence of minimal diaphragmatic contraction. If necessary, adjust the sweep speed; two breaths are used to assess for TFdi. In the absence of clear peak inspiratory thickness, the timing of inspiratory effort is determined clinically at the bedside. TFdi here is calculated as 11%, but would be averaged over a further two breaths (total of four breaths captured in two images). (B) Maximal diaphragm thickening fraction measured during maximal inspiratory efforts (TFdi,max) is stimulated either by coaching the patient to make maximal volitional efforts, or following a Marini mauver if the patient is unable to be coached and there is a P0.1 >2 cm H2O. TFdi,max is calculated here as 208%, however the largest value obtained after several (at least three) attempts would be recorded as the TFdi,max. There are pronounced difference in TFdi and Tdi during a maximal inspiration (B) compared to a minimal inspiratory effort (A). Please click here to view a larger version of this figure.
Following this protocol, diaphragm thickness and thickening fraction can be measured as noninvasive and reproducible means of evaluating diaphragm structure and function. Measurements can be made at the bedside and saved for blinded offline analysis. These measures can be obtained repeatedly over time to assess changes in diaphragm structure and function longitudinally.
In healthy adults, resting end-expiratory diaphragm thickness can range from 1.5 mm to 5.0 mm, depending on height, sex, and, probe position21. In healthy adults breathing at rest, tidal TFdi typically ranges between 15%-30%. During maximal inspiratory efforts, TFdi,max typically ranges between 30% and 130%13,21,22. Maximal TFdi <20% is diagnostic for severe diaphragm dysfunction13,21. Table 2 summarizes healthy and critically ill diaphragm thickness and thickening fraction.
Table 2: Reference values for diaphragm thickness and thickening fraction11,13,19,21,22,23,24,25,26,27,28,29,30,31,32. Please click here to download this Table.
In critically ill patients receiving invasive mechanical ventilation, baseline diaphragm thickness measured at the outset of respiratory failure is correlated to clinical outcome (higher baseline Tdi predicts lower mortality and faster liberation from mechanical ventilation). In these patients, the subsequent evolution of Tdi over time varies widely between patients. About 40%-50% of patients develop atrophy (a decrease in Tdi from baseline by more than 10%) within the first week of mechanical ventilation15. A small subset of patients exhibit a rapid early increase in Tdi exceeding 10% of baseline, possibly indicative of injury, inflammation, or edema in the muscle (but not muscle hypertrophy, since hypertrophy takes weeks to occur). TFdi,max <30% predicts a higher risk of failed weaning from mechanical ventilation23.
In the example shown in Figure 2A, diaphragm thickness in the first breath (in yellow) was 1.20 mm at end expiration and 1.51 mm at peak inspiration. The thickening fraction can then be calculated using the formula below and expressed as a percentage.
Diaphragm ultrasound provides a noninvasive, reliable, and valid technique to monitor diaphragm structure and function in healthy subjects and critically ill patients. Diaphragm thickening fraction provides a bedside measure of diaphragm contractile activity and function that is much more feasible than magnetic twitch transdiaphragmatic pressure measurements, the traditional gold standard method for evaluating diaphragm function33. Monitoring diaphragm function and thickness by point-of-care ultrasound provides a means of detecting diaphragm atrophy. As such, experts recommend a minimum of 15 separate transdiaphragmatic ultrasounds be performed and analyzed to develop competency17.
To ensure reproducible and precise measurements, it is imperative to mark probe placement19. The B-mode image should be optimized by adjusting the probe placement, as well as the depth, gain, and focus of the instrument. The sweep speed of the ultrasound used should be adjusted to obtain a minimum of two breaths within a captured image if possible. Lastly, measurements should be repeated until consistent values (within 10%) are obtained.
Some of the difficulties associated with obtaining Tdi and TFdi are the placement and orientation of the linear probe. Table 1 highlights some common scenarios and the associated troubleshooting measures users should undertake.
Some limitations of this ultrasound technique need to be noted. First, diaphragm thickness varies widely between patients, and changes in thickness over time need to be referenced to the baseline value (for example, to diagnose atrophy). Second, despite the simplicity of the technique, training is required to ensure competency. A web-based online training platform has been validated to achieve competency in the technique18. Third, the ultrasound technique described provides limited data on muscle structure (mass) and function (contractility). New techniques, such as shear ultrasonography and ultrasound elastography, can provide additional information concerning muscle stiffness and fibrosis34,35,36,37,38.
In summary, transdiaphragmatic ultrasonography provides key measures of diaphragm structure and function that can easily be performed in healthy and critically ill patients. This technique is reliable and valid, considering a competent user with sufficient training. This article outlines how to perform transdiaphragmatic ultrasound and cautions users to undergo sufficient training before data acquisition.
The authors have nothing to disclose.
10-15 MHz linear array transducer | Philips | L12-4 | Any 10-15MHz linear array transducer may be used |
Any DICOM viewer software Example: MicroDicom DICOM viewer | MicroDicom | Free for non-commerical use analysis software: https://www.microdicom.com/company.html | |
Lumify Ultrasound Application | Philips | Other systems will use their own software | |
Lumify Ultrasound System | Philips | Any ultrasound system may be used | |
Skin Safe Marker | Viscot | 1450XL | Used for marking location of probe |
Ultrasound Gel | Wavelength | NTPC201X | Any ultrasound gel may be used |