Diaphragmatic Ultrasound in Adults: Image Acquisition and Interpretation

Summary

Point-of-care ultrasound (POCUS) is an essential technique for screening for diaphragmatic dysfunction due to its portability, non-invasiveness, and real-time imaging capabilities. Although current diaphragmatic POCUS protocols exist, they suffer from poor interoperator reliability and lack consensus guidelines. Here we describe a technique that is reproducible and simple to perform.

Abstract

Diaphragm dysfunction is a widely recognized concern across numerous medical specialties and clinical settings. Timely and accurate assessment of the diaphragm is vital not only in critically ill patients, where it has a role in weaning from mechanical ventilation and respiratory outcomes, but also in the perioperative arena as a diagnostic tool to detect phrenic nerve function. Diaphragmatic assessment has traditionally utilized fluoroscopy and nerve studies that are time-consuming, costly, and non-portable. Point-of-care ultrasound (POCUS) overcomes these barriers and can be used as a tool for non-invasive screening of diaphragm function. However, POCUS for diaphragmatic dysfunction currently suffers from several issues such as a lack of consensus guidelines, a multiplicity of protocols, and poor interoperator reliability among existing protocols, most notably with the assessment of dome of diaphragm excursion and diaphragmatic thickening. To address these issues, this manuscript reviews the available literature on diaphragmatic POCUS and identifies an image acquisition technique that is both simple to perform and has high interoperator reliability. This technique first describes a qualitative evaluation of diaphragm excursion, followed by a quantitative assessment of the excursion of the zone of apposition. The technique is described stepwise along with all the following: patient positioning, transducer selection, probe placement, image optimization, and interpretation.

Introduction

Diagnostic ultrasound can be separated into two divisions: consultative and point-of-care. Consultative ultrasound incorporates an exam performed by a distinct specialist team, whereas POCUS is both performed and interpreted by the clinician caring for the patient in real time¹.

Over the past few decades, diagnostic POCUS has emerged as a transformative tool in modern medicine, with applications rapidly expanding across specialties. These POCUS applications are driven by ultrasound's noninvasive nature, portability, and real-time imaging capabilities. Further, within diagnostic POCUS, the applications that have achieved the highest uptake in clinical medicine tend to have both reasonably high accuracy compared to a gold standard and high interobserver reliability^2,3. For instance, POCUS of the lung is well established to narrow the differential diagnosis of respiratory insufficiency and has clear evidence-based guidelines supporting its standardized use⁴. However, while POCUS of the lung is well established, there remains an unmet need to develop a reproducible sonographic assessment of the diaphragm.

Such a non-invasive diaphragmatic assessment protocol would benefit multiple specialties and clinical situations, including but not limited to, critical care, pulmonology, perioperative care (including both general-purpose anesthesia and subspecialty regional anesthesia contexts), and neurology. In the intensive care unit, diaphragmatic dysfunction is a common concern, often arising from multiple underlying pathologies such as neuromuscular diseases, critical illness myopathy, trauma, and malnutrition⁵. Critically ill patients are often at high risk for both impaired contraction of the diaphragm and under-recognition of this phenomenon⁶. Further, diagnosing diaphragmatic dysfunction early is important, as not only can it assist in ventilation management strategies, but also dysfunction may be an early indicator of infection and sepsis^7,8. In addition, prolonged intubation can lead to significant morbidity, mortality, and increased healthcare expenses². In these scenarios, a noninvasive, portable protocol for diaphragmic assessment could be useful to assess the appropriateness for weaning from mechanical ventilation, evaluate work of breathing, and predict the probability of extubation success versus failure^6,8,9,10,11.

Within regional anesthesia, diaphragmatic POCUS could have value in screening for diaphragmatic paresis related to transient phrenic nerve dysfunction from brachial plexus blocks. Although tolerated well by healthy patients, phrenic nerve palsies can lead to respiratory distress in patients with limited pulmonary reserve. Furthermore, in the perioperative arena, POCUS of the diaphragm can serve as a diagnostic tool for patients in the preoperative, intraoperative, and postoperative settings. For example, diaphragmatic POCUS could be used to detect phrenic nerve damage arising from a wide range of procedures, including but not limited to, coronary artery bypass grafting with internal mammary artery harvesting, atrial fibrillation ablation, and cervical or thoracic surgeries^3,12.

Finally, within the specialty of neurology, POCUS could facilitate the assessment of diaphragmatic function in neurologic diseases such as Myasthenia gravis, Duchene's muscular dystrophy, amyotrophic lateral sclerosis, and cerebrovascular accidents¹³.

Accurate assessment of the diaphragm is essential due to its vital role in reparatory function. Oxygenation and ventilation depend on the generation of negative intrathoracic pressure created by the diaphragm, a dome-shaped muscle separating the abdomen and thorax that is composed of several muscular and tendinous membranes^14,15. The diaphragm has at least two major components that can be distinguished on ultrasound: the dome of the diaphragm (DoD) and the zone of apposition (ZOA). The DoD is the central tendinous portion that exhibits a hyperechoic and curved appearance on ultrasound. The ZOA is the lateral portion of the diaphragm that attaches to the rib cage and consists of muscular fibers that run parallel and proximal to the inner surface of the chest wall^3,15. The ZOA is thin (usually <1 cm in thickness), but it increases in thickness during inspiration as the diaphragm contracts. At the ZOA, the diaphragm has a characteristic appearance on ultrasound with three layers, including an anechoic muscular layer that is bounded externally by the superficial hyperechoic parietal pleural and internally by the deep hyperechoic peritoneum^3,13.

Several noninvasive sonographic protocols have been proposed for diaphragmatic assessment, involving both qualitative and quantitative approaches. Qualitative visual assessment, the simplest approach, entails the evaluation of diaphragmatic motion bilaterally, during either tidal or vital capacity breathing, using two-dimensional ultrasound, also known as Brightness mode (B-mode). In contrast, quantitative protocols typically begin with B-mode and add one-dimensional ultrasound -- also known as Motion Mode (M-mode) -- to measure one of two things: the excursion of the dome of diaphragm (DoD) and/or Diaphragmatic thickening^2,3,5,13. Measurement of DoD excursion is performed with a low-frequency transducer with the ultrasound beam directed through the posterior third of the hemidiaphragm at a perpendicular angle. M-mode is then utilized to measure excursion during vital capacity breathing.

Alternatively, the measurement of diaphragmatic thickening employs a high-frequency linear transducer in two steps. First, the high-frequency transducer is placed along the patient's flank overlying the diaphragm with B-mode to identify the zone of apposition (ZOA)³. Second, estimation of diaphragmatic thickening is performed using M-mode by measuring diaphragmatic thickness (in millimeters) from the visceral to parietal pleura and calculating the change in thickness by the following equation^2,3,5,13:

Change in thickness = (Thickness at end inspiration - Thickness at end expiration) / Thickness at end expiration

However, quantitative methods (DoD excursion and diaphragmatic thickening) suffer from poor interoperator reliability. Interoperator reliability is low for the measurement of DoD excursion for several reasons. First, providers have difficulty finding a consistent angle of visualization of the excursion of the dome of the diaphragm³. Second, assessing on the left side is frequently challenging due to the small acoustic window through the spleen^2,16. For example, studies have cited that identification of left-sided diaphragmatic excursion is not possible in up to 65-79% of cases¹⁷. Third, intraabdominal contents and patient positioning can influence the range of diaphragm excursion².

Similarly, the measurement of diaphragmatic thickening has low interoperator reliability for at least two reasons. First, the natural thinness of the diaphragm causes millimeter errors in measurement to be consequential. Second, the diaphragm's variability in thickness across rib interspaces and by the patient's laterality further causes measurement dispersion^2,3,17. In acknowledgment of these many limitations, in 2022, an expert consensus on diaphragm ultrasonography in critically ill patients concluded that current methods were not standardized and that many required a skilled sonographer¹⁸. They noted there was no agreement on cutoff values for diaphragm dysfunction based on thickening fraction and that measurement of thickening fraction is a difficult skill with a steep learning curve^13,18. Furthermore, the use of multiple different sonographic protocols in literature has added to inherent challenges by making the comparison of studies difficult, leading to heterogeneity in research¹⁹.

To address these issues, this manuscript reviews the available literature on diaphragmatic POCUS and identifies an image acquisition technique that is both simple to perform and has been shown to have high interoperator reliability. This feasible yet effective protocol begins with a qualitative evaluation of diaphragmatic excursion, followed by a recently validated quantitative assessment of excursion of the cranial-most point of the ZOA^17,19.

Protocol

All procedures performed in studies involving human participants were in accordance with the ethical standards of the Duke University Health System institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Informed consent was obtained from all participants. Supplemental File 1 contains the most important still images from each video.

1. Phase 1: Qualitative assessment of diaphragmatic excursion (Visual screening for gross hemidiaphragmatic dysfunction)

1. Machine setup and patient positioning
   1. Probe selection: Select a low-frequency (≤ 5 MHz) transducer (curvilinear or sector array [aka "phased-array"]¹⁹.
   2. Apply ultrasound coupling gel to the probe.
   3. Instrument settings: Select abdominal preset.
   4. Position the patient in the semirecumbent position.
2. Scanning technique
   1. Right hemidiaphragm assessment
      1. Place the probe on the right flank, 5-7^th intercostal space, mid-axillary line with the beam aligned with the coronal plane of the body and probe indicator pointing cranially (Figure 1 and Figure 2A).
      2. Adjust the probe positioning (slide, fan, rock as needed) until the view is centered on the diaphragm with the following structures also visible: sub-diaphragmatic organ (liver or spleen), diaphragm, spine, and supra-diaphragmatic space (i.e., pleural space)¹⁹ (Figure 2B,C).
      3. Ask the patient to take a slow vital capacity breath in and a slow breath out.
      4. Click Acquire (or equivalent) to capture a short clip during patient respiration.
      5. Visually assess diaphragmatic excursion as one of the following: Grossly intact (Video 1 and Video 2), Grossly absent (Video 3 and Video 4), or Indeterminate (Video 5 and Video 6).
      6. If indeterminate or further quantification is needed, proceed to section 2 (Phase 2) of the protocol.
   2. Left hemidiaphragm assessment: repeat steps 1.2.1.1-1.2.1.6 on the patient's left side.

2. Phase 2: Quantitative assessment of ZOA excursion

1. Machine setup and patient positioning
   1. Probe selection: Select a high-frequency (>10-13 MHz) linear transducer.
   2. Apply ultrasound coupling gel to the probe.
      1. Instrument settings: Select musculoskeletal (MSK) preset if available. If MSK preset is not available, select any preset and use the same preset for all high-frequency diaphragmatic scanning.
   3. Position the patient in the semirecumbent position (repeat step 1.1.4).
2. Scanning technique
   1. Right hemidiaphragm assessment
      1. Place the probe at the mid-axillary line at the level of the eighth or ninth intercostal spaces, with the probe indicator pointing cephalad towards the patient's head (Figure 3 and Figure 4A).
      2. Angle the beam perpendicular to the chest wall and center the axis so that the rib interspace is centered in the screen with the cranial and caudal ribs visible on the edges of the screen (Figure 4B).
      3. Set the depth such that the pleural line or diaphragm is visible in the middle third of the screen.
         NOTE: Typically, this means a depth of 3-5 cm but can be greater if there is additional subcutaneous tissue.
      4. Set the gain such that the diaphragm/pleural line are visibly distinct from surrounding structures.
      5. Identify the pleural line on the screen.
      6. Measure the end-inspiratory location of the ZOA.
         1. Give the patient the following instructions: "Breathe in fully and then hold your breath in for 4 s. If you cannot tolerate 4 s, then please hold your breath for any amount of time you're comfortable."
         2. During the patient's breath hold, follow the pleural line caudally until the location is reached where the pleural line is visible in only a portion of the rib interspace, and the remaining interspace contains the diaphragm at a similar depth as the pleural line (Video 7 and Video 8).
            NOTE: This rib interspace simultaneously containing pleura and diaphragm has been termed the Zone of Apposition (ZOA).
         3. Adjust the probe positioning (slide, fan, rock as needed) until the view is centered on the ZOA with the following structures also visible: the subcutaneous tissue above and a rib on either size of the screen (Figure 4C).
         4. Using a non-permanent skin marker, draw a line on the patient that is perpendicular to the ultrasound transducer's long axis and bisects the probe to mark the interspace where the ZOA was found (Figure 5A). The marking should be aligned with the ZOA, at the transition between the pleura and diaphragm (Figure 4B,C).
         5. Ask the patient to exhale and then "breathe normally" (aka tidal breathing).
         6. If unsure that one has identified the ZOA, repeat steps 2.2.1.6.1-2.2.1.6.3 and examine the presumed diaphragm in this view to see its changes during the respiratory cycle.
            NOTE: The true diaphragm should thicken during inspiration and decrease in thickness during expiration.
         7. Repeat the measurement once (i.e., steps 2.2.1.6.1-2.2.1.6.5).
         8. Take the average of the two measurements and use this for the final value of the end-inspiratory location of the ZOA (Figure 5B).
      7. Measure the end-expiatory location of the ZOA.
         1. Give the patient the following instructions: "Breathe in fully, then breathe out all the way, and then hold your breath out for 4 s. If you cannot tolerate 4 s, then please hold your breath for any amount of time you're comfortable."
         2. Slide the probe cranially to find the end-expiratory location of the ZOA.
         3. Repeat steps 2.2.1.6.3-2.2.1.6.4.
         4. Ask the patient to "breathe normally."
         5. Repeat the measurement once (i.e., steps 2.2.1.7.1-2.2.1.7.4).
         6. Take the average of the two measurements and use this for the final value of the end-expiratory location of the ZOA.
      8. Measurement of ZOA excursion
         1. Measure the distance between both the averaged end-inspiratory and averaged end-expiratory skin markings in cm with a ruler. The distance between the two external skin marking represents maximal diaphragmatic excursion (Figure 5C).
   2. Left hemidiaphragm assessment
      1. Repeat all the sub-steps contained within step 2.2.1 on the left chest.

Results

This diaphragmatic ultrasound protocol begins with the qualitative assessment of each hemithorax during a vital capacity breath to sort each hemidiaphragm into one of three categories: grossly intact excursion, grossly impaired excursion, or indeterminate. Examples of grossly normal vital capacity excursion of the right and left hemidiaphragms are shown in Video 1 and Video 2, respectively. Examples of grossly impaired vital capacity excursion of the right and left hemidiaphragms are sho...

Discussion

POCUS offers clear advantages for diaphragmatic assessment, including portability, non-invasiveness and real-time imaging capabilities. These strengths can be taken advantage of with this feasible and accessible protocol and can be applied in a variety of clinical settings. This protocol begins with a qualitative assessment of diaphragmatic excursion to answer the question of whether gross hemi-diaphragmatic dysfunction is present. If the answer is unclear or if more specific information is needed, the second step of the...

Materials

List of materials used in this article

Name	Company	Catalog Number	Comments
Medical Ruler	MediChoice	NA	We used Medichoice as that is what is readily available at our institution and it comes with the skin marker, however any medical ruler will work. The majority of skin markers come with a type of ruler or measurement system, but if not a separate ruler can be used.
Skin Marker	MediChoice	NA	We again used Medichoice as that is what is readily available at our institution and it comes with the ruler, however any standard skin marker will work.
Ultrasound Gel	Aquasonic	NA	Any standard gel will work. Sterile packs are not necessary but can be used on a case-by-case basis at the providers discretion.
Ultrasound Machine	Samsung and GE	NA	Any standard portable ultrasound machine will suffice.