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Assessing Diaphragmatic Function

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The diaphragm is vulnerable to injury during mechanical ventilation, and diaphragm dysfunction is both a marker of severity of illness and a predictor of poor patient outcome in the ICU. A combination of factors can result in diaphragm weakness. Both insufficient and excessive diaphragmatic contractile effort can cause atrophy or injury, and recent evidence suggests that targeting an appropriate amount of diaphragm activity during mechanical ventilation has the potential to mitigate diaphragm dysfunction. Several monitoring tools can be used to assess diaphragm activity and function during mechanical ventilation, including pressure-derived parameters, electromyography, and ultrasound. This review details these techniques and presents the rationale for a diaphragm-protective ventilation strategy.

• respiratory muscles
• muscle weakness
• intensive care
• diagnostic techniques
• respiratory system
• diaphragm dysfunction
• effort-induced lung injury
• Introduction

Patients who are admitted to an ICU frequently exhibit muscle weakness, and the respiratory muscles are often affected. 1 The diaphragm is the primary inspiratory muscle, and diaphragm dysfunction is both a marker of severity of illness and a predictor of poor patient outcome in the ICU. There is a clear association between diaphragm dysfunction and an increased risk of mortality or prolonged mechanical ventilation. 1 - 6 Factors related to both critical illness and ICU interventions are at the root of this problem. 7 Mechanical ventilation is associated with diaphragm injury through a variety of mechanisms referred to as myotrauma. 8 The presence of either insufficient or excessive diaphragmatic contractile effort plays a central role in this process. In addition, vigorous diaphragmatic contractions also can result in lung injury. 9 - 11 Recent evidence suggests that maintaining appropriate diaphragm activity during mechanical ventilation has the potential to prevent injury to the diaphragm. 6 These observations have drawn greater attention to the importance of diaphragm monitoring in the ICU.

Several clinical monitoring tools are available to assess diaphragm activity and function, including various respiratory pressure measurements, electromyography (EMG), and ultrasound. This paper briefly discusses the impact of critical illness on the diaphragm, with an emphasis on the effects of mechanical ventilation and diaphragm activity, and details the effect of diaphragm dysfunction on outcome. It will then discuss the relevant techniques for monitoring diaphragm function, with special reference to their application in mechanically ventilated patients.

• Respiratory Muscle Physiology

The diaphragm is a thin, dome-shaped muscle that inserts into the lower ribs, the xiphoid process, and the lumbar vertebrae, separating the thoracic and abdominal cavities. During inspiration, shortening of diaphragm muscle fibers results in a piston-like action, decreasing intrapleural pressure, drawing the lungs downwards, and increasing intra-abdominal pressure. The force generated by the diaphragm is quantified by the transdiaphragmatic pressure (P di ), which is the pressure gradient generated between the thoracic and abdominal cavities during diaphragm contraction. It is calculated from the difference between the pressure in the stomach (gastric pressure, P ga ) and the esophageal pressure (P es , as a substitute for intrapleural pressure): P di = P ga – P es . 12 - 14 Decreasing pleural pressure generates a pressure gradient that drives flow and volume into the lungs, known as the transpulmonary pressure. The transpulmonary pressure is computed as the difference between airway pressure (P aw ) and P es (ie, P aw – P es ). Of note, even though the P es is closely related to the pleural pressure, the pleural pressure varies over the lung surface due to the effects of gravity and regional mechanics. 15 This transpulmonary pressure drives alveolar ventilation and reflects the stress and strain applied to the lung by the respiratory muscles (and the ventilator).

Accessory respiratory muscles include the external intercostal, scalene, and sternocleidomastoid muscles. The external intercostal muscles pull the ribs upward and forward, increasing the lateral and anteroposterior diameters of the thorax. The scalene muscles elevate the first 2 ribs, and the sternocleidomastoids raise the sternum.

Exhalation is largely a passive process, except under conditions of increased respiratory load. 16 When the workload increases, the abdominal muscles contract during expiration, with an initial recruitment of transversus abdominis muscle and subsequent recruitment of the other abdominal muscles. 17 Expiratory abdominal muscle contraction enhances inspiratory diaphragm performance (through its length–tension relationship) and spring loads the thoracic cage to expand when the abdominal muscles relax, assisting with the inspiratory work of breathing. 18 The work of breathing during heavy loads is thus redistributed to accessory inspiratory muscles, abdominal muscles, and the diaphragm. Figure 1 summarizes the action of respiratory muscles and pressure relationships.

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Pressure model of the respiratory system. The locations of relevant pressures are depicted on the left. Typical tracings of respiratory pressures under assisted mechanical ventilation are shown on the right. P pl is estimated with esophageal manometry. The respiratory P mus is computed as the difference between observed P cw and ΔP es . P cw is estimated as the product of tidal volume and chest wall elastance measured during passive ventilation. P alv = alveolar pressure; P aw = airway pressure; P cw = chest wall elastic recoil pressure; P es = esophageal pressure; P ga = gastric pressure; P L = transpulmonary pressure (P aw – P es ); P mus = respiratory muscle pressure; P pl = pleural pressure. Adapted from Reference 19 .

• Causes of Diaphragm Weakness in the ICU

The causes and mechanisms leading to the observed weakness of the diaphragm in ventilated patients in the ICU have been extensively studied. We now know that there are multiple intertwined factors related to critical illness, ICU stay and therapies, and mechanical ventilation itself that are causing this weakness. The combination of these mechanisms causing diaphragm injury and weakness in the ICU is now called critical illness-associated diaphragm weakness. The precise mechanisms are thoroughly detailed in a recent review by Dres et al 7 and summarized in Figure 2 .

Schematic illustration of the mechanisms involved in the occurrence of critical illness-associated diaphragm weakness. Dashed lines represent uncertain causation; solid lines represent established causation. Adapted from Reference 7 .

Of specific interest for this article are the mechanisms of ventilator myotrauma, which are the deleterious effects of mechanical ventilation on diaphragm structure and function. Up to 4 distinct forms of myotrauma might occur during ventilation: ventilator overassistance, ventilator underassistance, eccentric (pliometric) diaphragm contractions, and excessive end-expiratory shortening. Interestingly, these mechanisms have the potential to be targeted by specific ventilation strategies, potentially mitigating the occurrence or severity of diaphragm myotrauma.

Overassistance myotrauma refers to the diaphragm atrophy resulting from excessive unloading of the respiratory muscles. 20 - 24 This form of injury is well documented in the clinical setting. It affects approximately 50% of ventilated patients and can be mitigated by preserving some degree of muscle activity during mechanical ventilation. 20 , 25 - 27

Underassistance myotrauma develops when respiratory effort is excessive because of insufficient unloading. 28 Experimental and clinical studies have demonstrated sarcomere disruption, tissue inflammation, and muscle fatigue. 29 - 31 Sepsis renders the muscle tissue particularly susceptible to this form of injury. 32 The observation that diaphragm thickness increases over time in some ventilated patients (in association with elevated respiratory effort) may reflect this edema and injury. 6

Eccentric diaphragm contractions developing during muscle fiber lengthening, that is, during the ventilator’s expiratory phase, can also cause injury (ie, eccentric myotrauma). Eccentric loading is considerably more injurious than concentric loading. This type of myotrauma can be the result of increased postinspiratory diaphragm activity in the expiratory phase (ie, expiratory braking), patient–ventilator asynchrony (particularly reverse-triggering), or even excessive accessory respiratory muscle activity moving the diaphragm cranially during inspiration. 33 , 34

Preliminary evidence also suggests the possibility that prolonged shortening of the diaphragm from elevated end-expiratory pressure may cause muscle fiber dropout and may allow longitudinal atrophy. 35 Abruptly decreasing PEEP may then put the diaphragm in a disadvantageous length–tension relationship at the beginning of inspiration. 36 The clinical relevance of this phenomenon is uncertain.

This brief summary of the mechanisms of diaphragm myotrauma suggests that routine monitoring of diaphragm activity and function might help clinicians prevent or mitigate myotrauma, potentially improving clinical outcomes.

• Monitoring Diaphragm Function and Activity

A range of techniques are available to monitor the diaphragm. Depending on the conditions under which they are measured, these techniques can be used to quantify either function (ie, force-generating capacity) or muscular contractile activity. Most tests of muscle function require a maximum volitional contractile effort from the patient. Some parameters actually reflect the performance of the respiratory system as a whole, not just the diaphragm. We will discuss the relevant techniques with special reference to their application in mechanically ventilated patients. These are summarized in Table 1 .

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Pressure-Based Monitoring Tools, EMG, and Ultrasound Parameters to Evaluate Diaphragm and Respiratory System Activity and Function

Respiratory System Pressures

Several techniques measure the pressures generated by the respiratory system as a whole or by the diaphragm alone ( Table 1 ). The maximum inspiratory pressure (P Imax ) can be measured at the airway while the patient makes a maximum inspiratory effort against a closed airway; this is frequently used as a test of respiratory muscle function. 37 A 1-way valve should be applied so that the patient can exhale but not inhale, thus minimizing lung volume to optimize the length–tension relationship of the diaphragm and maximize force generation. When both P ga and P es are recorded during this effort, maximum P di can be calculated to specifically evaluate the strength of the diaphragm. A related parameter is the pressure generated by all respiratory muscles (P mus ). By definition, P mus = (V T × E cw ) − ΔP PL , where V T is the tidal volume, Δ-P PL is the pleural pressure swing represented by Δ-P es , and E cw is the chest wall elastance. When the airway is occluded, P mus is equal to ΔP es and hence to ΔP aw .

With these techniques, it is critical to make sure that the patient is exerting maximum effort. This dependence on effort is the primary drawback of all volitional function tests. To circumvent this shortcoming, different strategies have been implemented. By stimulating the phrenic nerves with a magnetic or electric pulse (or twitch) while the patient is relaxed at end-expiration, a brief diaphragm contraction of standard magnitude is induced, independent of the patient’s effort. 37 Despite its technical challenges, this technique is the accepted standard for measuring diaphragm function in ventilated patients. 42 To obtain accurate values, a supramaximal stimulation of the phrenic nerves is needed, and positioning of the magnetic coils must be very precise. Similarly, twitch P aw can be recorded to provide a close estimate of twitch P di in ventilated patients. 42 , 43 Reference cutoff values defining diaphragm weakness are available and are summarized in Table 1 . Some have proposed lower cutoff values for twitch P aw for defining dysfunction in an ICU setting, based on the possibility of these values to better predict weaning outcome. 44

An alternative strategy to obtain maximum volitional effort for a functional measurement is to apply a 20-s airway occlusion with a 1-way valve (Marini maneuver), allowing for expiration but not inspiration. 45 The pressure obtained with this maneuver corresponds closely to the pressure obtained when patients are coached to breathe at maximum effort, provided that respiratory drive is adequate at rest (ie, P 0.1 >2 cm H 2 O).

Another technique to measure respiratory muscle strength in nonintubated patients is the sniff nasal inspiratory pressure (SNIP). Sniffing is an intuitive subconscious maneuver that elicits maximal diaphragmatic and respiratory muscle activation. Like the previously mentioned parameters, P es and transdiaphragmatic pressures can also be recorded during sniffing.

If the pressure is obtained during a tidal breath, the recorded pressure quantifies the effort exerted by the respiratory muscles or diaphragm. During inspiration, a negative deflection in esophageal pressures signifies respiratory muscle contraction. Figure 3 shows a sample of high and low inspiratory effort, documented with P es and P aw tracings. Small amounts of diaphragm activity may go unnoticed by only looking at the P es curve (ie, the amount of effort counterbalanced by chest wall recoil pressure, see Fig. 1 ), which may be detected with EMG monitoring. 46

Airway pressure (P aw ), esophageal pressure (P es ), and transpulmonary pressure (P L ) tracings of a patient with high (left) and low (right) inspiratory effort. High effort is demonstrated by a large drop in P es during inspiration.

The airway occlusion pressure (P 0.1 ), which is the pressure developed in the occluded airway 100 ms after the onset of inspiration, is an old parameter that may have a value in the assessment of a patient’s respiratory drive. 47 It can be obtained easily on most ventilators, and it is reliable in the setting of respiratory muscle weakness. 48 It correlates well with work of breathing (WOB) and the pressure–time product (PTP), 2 parameters that assess respiratory activity, so P 0.1 can reliably demonstrate excessive effort during various modes of ventilation and during extracorporeal membrane oxygenation. 49 - 52 Cutoff values indicating underassist have been proposed. Rittayamai and coworkers 51 defined the optimal threshold of P 0.1 at 3.5 cm H 2 O with a sensitivity of 92% and a specificity of 89% to detect underassist; others have set the optimal threshold for overassistance at ≤ 1.6 cm H 2 O.

The amplitude of swings in P di and P es do not fully reflect the amount of breathing effort a patient performs because the inspiratory time, frequency, and expiratory muscle activity are not taken into account. 53 The PTP is the integral of the pressure developed by the respiratory muscles during contraction (ie, P mus ) over time (specified as either per breath or per minute). When P di is measured, the specific PTP of the diaphragm can be quantified. Oxygen consumption by the respiratory muscles correlates well with the PTP, whereas it only weakly correlates with the mechanical WOB index mentioned above. 54 This could be due to the fact that PTP takes the isometric phase of muscle contraction into account.

Diaphragm EMG

Diaphragm EMG can be used to assess diaphragm activity. Either surface EMG for the costal diaphragm or esophageal recordings of the crural diaphragm can be used. Needle EMG studies are rarely used to monitor diaphragm activity for clinical monitoring, but they can be useful in the assessment of neuropathy and myopathy. The EMG-derived parameters are summarized in Table 1 .

EMG provides the best clinically available representation of the integrated neural output of the brain’s respiratory center; changes in EMG values are linearly correlated with changes in CO 2 levels. 52 , 57 A specialized nasogastric tube with electrodes positioned at the diaphragm can be used to measure the crural diaphragm electric activity (EA di ). A specific mode of ventilation called neutrally adjusted ventilatory assist uses this measurement to synchronize diaphragm EMG with the ventilator. The peak of the EA di signals per breath and EA di values during maximum inspiratory effort can be recorded. Some elements need to be taken into account to understand the relationship between diaphragm EMG, respiratory drive, and diaphragm force. One of the elements is the neuromuscular efficiency, which is the relationship or coupling between EA di and P di (ie, the pressure generated by the diaphragm). By definition, the neuromuscular efficiency index is P di /EA di (cm H 2 O/mcV). This index is patient-specific and can change over time. 58 , 59 As a result, neuromuscular efficiency can only be used to estimate the breathing effort and diaphragm function on an individual basis because reference values are nonexistent. 58 In a study by Liu et al, 60 subjects who passed a spontaneous breathing trial exhibited higher neuromuscular efficiency values than those who failed the spontaneous breathing trial.

Diaphragm ultrasound has gained popularity in the last decade because it enables clinicians to directly and noninvasively assess diaphragm activity and function. The diaphragm can be visualized in 2 ways, either in the zone of apposition or via a subcostal anterior approach. There are excellent reviews on the technical details and validity of these techniques, summarized in Table 1 . 61 , 62 When the diaphragm contracts and shortens, the muscle thickens, and this thickening can be visualized on ultrasound ( Fig. 4 ). The increase in thickness during contraction (quantified as the thickening fraction) reflects diaphragm contractile activity and correlates with other parameters of diaphragm activity, like EA di and PTP. 62 , 64 The maximum thickening fraction correlates with twitch P aw and provides an estimate of diaphragm function. 44 , 65 , 66 The technique can also be used to detect structural changes in the diaphragm during mechanical ventilation, such as diaphragm atrophy, load-induced injury, or recovery of muscle mass. 6 , 20 , 23 , 67

M-mode ultrasound images of the diaphragm measured at the zone of apposition, and measurements of the thickness (blue vertical lines) during expiration (distance 1) and inspiration (distance 2). (A) Undersupport with a thickening fraction of 150%: ([0.55 − 0.22 cm] × 100)/0.22 cm. (B) Oversupport with a thickening fraction of 4%: ([0.25 − 0.24 cm] × 100)/0.24 cm. (C) Adequate support with a thickening fraction of 38%: ([0.36 − 0.26 cm] × 100)/0.26 cm. Reprinted from Reference 63 , with permission.

As discussed earlier, a maximum inspiratory effort is required to assess diaphragm function (ie, maximum thickening fraction). A maximum inspiratory effort can be elicited by coaching or by the Marini maneuver (described above). However, because thickening results from muscular shortening, occluding the airway during the inspiratory effort can artefactually reduce thickening. Consequently, if a prolonged 20-s occlusion is applied to maximize inspiratory effort, maximal thickening should be measured only once the occlusion is released (but shortly after so that respiratory effort is still elevated).

Diaphragm excursion (motion) can be quantified when looking at the diaphragm subcostally ( Fig. 5 ). These measurements provide a well-validated method of assessing diaphragm function. Importantly, interpretation of the result is only possible during unassisted breaths because downward displacement during assisted breaths could be a result of passive lung inflation by the ventilator. Therefore, the excursion cannot be used to monitor effort during mechanical ventilation. Diaphragm weakness will result in reduced caudal excursion, and paresis will often result in cranial (paradoxical) excursion during inspiration. 67 Vigorous accessory respiratory muscle activity moving the diaphragm cranially during inspiration could theoretically give falsely low values for this parameter. 34 Cutoff values for the diagnosis of diaphragm dysfunction using these techniques are summarized in Table 1 .

B-mode (right) and M-mode (left) ultrasound images of the diaphragm with a probe positioned subcostally. A downward diaphragm excursion during inspiration (ie, towards the ultrasound probe) is visible. Reprinted from Reference 68 , with permission.

• Balancing Over- and Underassistance

There is uncertainty about the optimum range of diaphragm activity during mechanical ventilation, but the avoidance of excessive activity when possible appears to be supported by recent evidence. Several parameter values have been proposed to demonstrate underassistance, including PTP and WOB. Table 2 summarizes the possible monitoring techniques to assess patient and ventilator breath contribution and to balance over- and underassistance.

Available Parameters to Evaluate Ventilator Over- and Underassist

The diaphragm is vulnerable to injury during mechanical ventilation, and a range of factors can impact its function. Among these factors, the effects of mechanical ventilation require close attention as they are potentially avoidable. Several mechanisms link mechanical ventilation with diaphragm injury, including excessive and insufficient respiratory support, which can lead to very high or low respiratory effort. In addition to the effects on the diaphragm itself, inappropriate respiratory muscle effort is also associated with lung injury, patient–ventilator asynchrony, and poor sleep quality. Furthermore, recent evidence has indicated that diaphragm dysfunction by itself has a strong impact on patient outcome. As a consequence, the assessment of diaphragm function and activity during mechanical ventilation has gained importance in the ICU setting. Several methods are available, including pressure-based parameters, EMG, and ultrasound. Depending on their specific use, these methods can evaluate strength (ie, function) or measure activity. Using these tools, the potential to balance diaphragm activity and to combine diaphragm- and lung-protective elements in a novel ventilation strategy has emerged. Future research will need to further detail these elements and define safe margins for diaphragm activity. For those reasons, a good understanding of monitoring tools is needed, and building expertise into at least one of them is useful for the bedside clinician.

It’s amazing work you’ve performed, and we use it a lot in our daily practice. I always struggle with the precision of the measurements because we’re talking about something that’s 2 mm and so whether you have a 20% variation, let’s say it goes from 2 to 2.4 mm and sometimes the precision of your caliper is not that good. If you go just one pixel above or below you will have very different impressions. How do you take that into account when you measure, and how do you make sure that what you measure is what you see on the screen?

An excellent point, Tài. In a lot of the early work we did looked at measuring ability and reproducibility with the technique, we found that you could get very good reproducibility of end-expiratory thickness measurements, the thickness of the muscle with reproducibility of ± 0.2 mm when the technique was optimized. However, the reproducibility of the thickening fraction, because it’s really the combination and ratio of 2 different thickness measurements (and therefore combines the error of both measurements) is suboptimal; ±16–20% is what we showed. There’s no question that it’s an imperfect technique for monitoring inspiratory effort from that standpoint, you’re going to have noise. You’ll be able to distinguish between a patient who’s not making any effort, a patient making low effort like a healthy subject, a patient making elevated effort, and a patient making very high effort. But in terms of a change from 10% vs 20% I wouldn’t call that physiologically significant just given the measurement noise. Nevertheless, this does a couple of things. First of all, it means the technique really starts to shine whenever you’re able to make measurements in large groups of patients where the signal/noise ratio can become clearer. Really the exciting advance of the technique is that it allows you to assess the diaphragm in large numbers of patients because it’s so feasible. Secondly, I think it’s questionable whether this is the answer in terms of driving our monitoring of respiratory effort at the bedside. Should we be using thickening fraction to decide how much pressure support is best so that the patient is in the optimum window? Personally, I think it’s not quite feasible enough, it takes 5–10 minutes to set up, you have to find the diaphragm, and until if and when somebody develops a probe that sits there continuously and can make measurements, I’m not sure it’s sufficiently easy to implement, never mind the reproducibility. In my view, things like airway occlusion pressure or the occlusion pressure technique described here or EAdi or other pressure-based techniques for monitoring have a lot more potential to guide diaphragm-protective ventilation, but I’m still amazed by how much we’ve been able to learn from a technique that’s not perfect.

How important is the diaphragm condition at the beginning of mechanical ventilation in terms of injury. Should we use different protective mechanical ventilation strategies? Should we use more spontaneous breathing or less sedation?

This is my personal bias, but I really think this should be considered in every patient who’s on a ventilator, because in our cohort study subjects were at similar risk of diaphragm atrophy across the range of diagnoses whether it was acute hypoxemic respiratory failure or post-transplantation or all different admission diagnoses. I think it’s something we need to consider with every ventilated patient, it’s a little different than even lung protection, which primarily we think about in ARDS. Granted, we do think about lung protection in other patients. First, a diaphragm-protective approach should be considered in most patients. Second, in order to implement a diaphragm-protective approach, it’s not going to just change how we set the ventilator, it’s going to change how we apply sedation, it will change which sedatives we use, and so on. We actually just organized a consensus meeting in Milan with the Pleural Pressure Working Group to get together and think about all these kinds of issues because it’s a completely different paradigm for how to manage respiratory failure. In terms of concerns about load-induced injury, the concerns about this apply even before the patient is intubated. How much load-induced injury are patients developing while we’re sitting there trying to decide whether to intubate them and put them on a ventilator or not?

This links with breathing frequency and effort. Before mechanical ventilation initiation, usually frequency changes little while effort increases.

Exactly. That’s a very important point. Frequency really doesn’t reflect effort levels very well at all.

I think the future is interesting, so I’ll be very attentive to where this work goes in topics connected to this conference. What Lluís [Blanch] was asking about, you have this information and you showed this great figure of 3 groups, those who had a thickening at the onset of mechanical ventilation, those that maintained that thickening, and those who lost thickness. I understand it’s going to be a little bit speculative, but I’d be interested to hear your vision for what that’s going to be at the bedside. One such case may be, ‘hey this person has been dwindling on the floor because the clinician didn’t count the frequency properly, missed signs of respiratory distress and this poor soul has been working like a dog… let’s rest them for a period of time and allow their diaphragm to recover.’ Or perhaps there’s another group who will be susceptible to rapid onset diaphragmatic atrophy in the ICU. I’m interested to hear your thoughts as to where this may go.

I think we need to do a huge amount of work to understand which patients we need to be most attentive to these issues in, and what the relative balance of protecting the lung versus protecting the diaphragm is because the two issues sometimes compete. Sometimes you have a completely suppressed respiratory effort in order to minimize tidal volume, and at that point you’re sacrificing the diaphragm in order to protect the lungs. The timing of which organ you prioritize and when is an important issue that needs to get sorted out. I would say in general we should be targeting a relatively low-normal level of effort in all patients from the moment of intubation essentially. Whether or not that’s feasible is a different question because there are sometimes reasons why respiratory effort needs to be suppressed. We’re now running a pilot feasibility physiological trial where we’re trying to take subjects at a very early stage and see if we can get their respiratory effort into a protective range. The idea would be really that everyone should be breathing at a low-normal level of effort as seen in healthy subjects unless there’s some good reason why the case should be otherwise.

What is the timeframe and magnitude of recovery?

That’s an interesting question that actually needs to be described. I’ve seen data from a group in Italy as well as some of our data, where some patients will recover diaphragm thickness almost as rapidly as they lost it and in others it seems to persist. There are so much data that we haven’t had time to analyze and write it all up, but that’s an important project waiting to happen. In animal models, the muscle can recover very quickly after the reinstitution of respiratory effort. It’s probably not that big of a deal to have a patient apneic for a couple of days, but as soon as they’re allowed to breathe we should try to make sure that the muscle is active at the protective level to try and restore function. But it’s a great question that needs more study.

If the recovery potential is so high, would that argue more for protecting the lungs over the diaphragm?

I think so, for sure. There’s no question that lung injury drives mortality, we know that from ARDSnet and other trials – I’m not claiming that diaphragm injury necessarily drives mortality. We’ve found a very weak association with mortality. However, patients may survive but then will be stuck on the ventilator for a prolonged period of time because of myotrauma and then develop other nosocomial badness from the prolonged mechanical ventilation and then experience the devastating functional sequelae of critical illness – in my view, intervening on myotrauma has the potential to change long-term functional outcomes. It may not change survival per se.

The question is which is the worst asynchrony for diaphragm injury?

Ask Tài [Pham].

I have no answer, ask Laurent Brochard.

It’s hard to answer confidently, but there are several ways in which asynchrony may be injurious to the diaphragm. And probably the most important way is by inducing eccentric contractions of the muscle, these are contractions that occur while the muscle is lengthening rather than shortening. Usually when you’re using your diaphragm, the inspiring muscle is shortening and lung volume is increasing. But, for example, in reverse triggering the muscle often reaches peak contractile activity after the ventilator has already cycled into expiration, so lung volume is actually decreasing. The dome of the diaphragm is rising and then the diaphragm is forced to contract while it’s rising and that induces eccentric contractile conditions. It’s a well-established principle of exercise physiology that if you want to train a muscle you do so by injuring it and the best way to injure it is with an eccentric contraction, that’s why when you lift weights to strengthen your biceps, you really want to contract that bicep as you’re lowering the weight because that’s where the injury stimulus for hypertrophy occurs. It’s the same with the diaphragm. Of course because you’re repeating it over for hours and hours it becomes very injurious rather than having a training effect. A similar circumstance we might be familiar with eccentric contraction is after a day of skiing and the next day your quads are screaming in pain, it’s because you were having eccentric contractions in your quadriceps all day the day before. There are very limited experimental data showing that eccentric contractions are fairly injurious to the diaphragm. I’m aware of some data from a group in Toronto, who found it may be profoundly injurious to the diaphragm, but this needs to be studied more. The principle is that anything that causes an eccentric contraction, even short cycling where a patient is in the middle of an inspiratory effort and all of a sudden the ventilator stops delivering inspiratory support and the patient is stuck, that could be profoundly injurious as well.

On the subject of eccentric contraction, it is certainly injurious but beyond the type of asynchrony it’s also the magnitude of the efforts that may be important. This reverse triggering, after passive insufflation depending on the timing might have a different impact. And if the peak is before inflation, maybe it will maintain your diaphragm function by having some contractions rather than remaining totally passive. But it’s a hypothesis only; we have no proof.

I’m sure you’ve seen the idea of pacing the diaphragm. A lung pacer company has proposed a clinical trial (Percutaneous Temporary Placement of a Phrenic Nerve Stimulator for Diaphragm Pacing (RESCUE1) ClinicalTrials.gov Identifier: NCT03107949 ). What do you think about doing pacing of the diaphragm, regardless of the method by which you do it? To me it seems clear that pacing a diaphragm that has disuse atrophy is going to be completely different than pacing a diaphragm in a septic patient or a patient who has respiratory muscle weakness.

Great question. There are certainly data that show that phrenic nerve stimulation in human subjects during cardiac surgery can protect mitochondrial function in the muscle, in the diaphragm for example. So there is a lot of biological plausibility for the technique. I think the question is in whom should we do this? It needs to be in a patient in whom you otherwise cannot optimize mechanical ventilation to achieve a reasonable respiratory effort level. It’s somebody who will have to be heavily sedated for at least 24 h in order to be a patient who could benefit from the intervention. But also they can’t be pharmacologically paralyzed because this kind of phrenic nerve pacing really doesn’t achieve any effect. It’s an ongoing question of exactly who is the most likely to benefit. In the group of patients with sepsis in whom the muscle becomes very vulnerable and fragile to mechanical stresses, you might well be doing more harm than good. You’d probably have to generate a high-normal level effort levels in order to achieve much injury, pacing at a low effort level might still be safe in these patients but that’s an important subgroup that needs to be studied.

My question is regarding ineffective efforts. In pressure support, excessive assistance is accompanied with ineffective inspiratory efforts but not dyspnea. The contrary happens in conditions of insufficient assistance where there are not ineffective efforts because respiratory drive is increased but at considerable dyspnea.

I’m not sure how injurious ineffective efforts are because most of the time the effort levels during ineffective efforts are really quite small. I assume you agree with me on that?

I think like Tài pointed out it’s a dose-dependent phenomenon and if the effort levels are very small even if the contractile conditions are potentially injurious it’s probably not that big of a deal.

Maybe the point is comfort. Vitacca et al 1 tested different levels of pressure support and PEEP showed a U shape relationship between excessive dyspnea without ineffective efforts and no dyspnea with increased hyperinflation and ineffective efforts. Perhaps a balance between the two is clinically acceptable.

• Acknowledgment

We thank Jose Dianti MD, for his help in designing the figures.

• Correspondence: Ewan C Goligher MD PhD, Toronto General Hospital, 585 University Ave, Peter Munk Building, 11th Floor, Room 192, Toronto, Ontario, Canada M5G 2N2. E-mail: ewan.goligher{at}utoronto.ca

Dr Schepens is supported in part by the European Respiratory Society, Fellowship STRF October 2018. Dr Goligher is supported by an Early Career Investigator Award from the Canadian Institutes of Health Research, and he has disclosed a relationship with Getinge. Ms Fard has disclosed no conflicts of interest.

Dr Goligher presented a version of this paper at the 58th R espiratory C are Journal Conference, held June 10–11, 2019, in St Petersburg, Florida.

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• Published: 22 October 2021

Diaphragmatic excursion is correlated with the improvement in exercise tolerance after pulmonary rehabilitation in patients with chronic obstructive pulmonary disease

• Masashi Shiraishi   ORCID: orcid.org/0000-0001-5410-1331 1 , 2 ,
• Yuji Higashimoto 1 ,
• Ryuji Sugiya 1 ,
• Hiroki Mizusawa 1 ,
• Yu Takeda 1 ,
• Shuhei Fujita 1 ,
• Osamu Nishiyama 2 ,
• Shintarou Kudo 3 ,
• Tamotsu Kimura 1 ,
• Yasutaka Chiba 4 ,
• Kanji Fukuda 1 ,
• Yuji Tohda 2 &
• Hisako Matsumoto 2  

Respiratory Research volume  22 , Article number:  271 ( 2021 ) Cite this article

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In patients with chronic obstructive pulmonary disease (COPD), the maximum level of diaphragm excursion (DE max ) is correlated with dynamic lung hyperinflation and exercise tolerance. This study aimed to elucidate the utility of DE max to predict the improvement in exercise tolerance after pulmonary rehabilitation (PR) in patients with COPD.

This was a prospective cohort study. Of the 62 patients with stable COPD who participated in the outpatient PR programme from April 2018 to February 2021, 50 completed the programme. Six-minute walk distance (6MWD) was performed to evaluate exercise tolerance, and ultrasonography was performed to measure DE max . Responders to PR in exercise capacity were defined as patients who demonstrated an increase of > 30 m in 6MWD. The receiver operating characteristic (ROC) curve was used to determine the cut-off point of DE max to predict responses to PR.

Baseline levels of forced expiratory volume in 1 s, 6MWD, maximum inspiratory pressure, DE max and quadriceps muscle strength were significantly higher, and peak dyspnoea of modified Borg (mBorg) scale score was lower in responders (n = 30) than in non-responders (n = 20) to PR (p < 0.01). In multivariate analysis, DE max was significantly correlated with an increase of > 30 m in 6MWD. The area under the ROC curve of DE max to predict responders was 0.915, with a sensitivity and specificity of 83% and 95%, respectively, at a cut-off value of 44.9 mm of DE max .

DE max could adequately predict the improvement in exercise tolerance after PR in patients with COPD.

Chronic obstructive pulmonary disease (COPD) is a progressive disease characterised by minimally reversible airflow limitation [ 1 ]. The main feature of COPD is the inability of patients to cope with their activities of daily life due to shortness of breath. Although the pathophysiological mechanisms involved in the development of dyspnoea and poor exercise tolerance in patients with COPD are complex, dynamic lung hyperinflation (DLH) plays a central role [ 2 ] by increasing ventilatory workload and decreasing the pressure-generating capacity of the inspiratory muscles.

Pulmonary rehabilitation (PR) is a non-pharmacological intervention and has been reported to improve dyspnoea, exercise capacity and quality of life of patients with COPD [ 3 ]. Owing to a body of evidence, PR is now established as the standard of care for patients with COPD [ 4 ]. However, not all patients with COPD benefit from PR to the same extent. Therefore, identifying patients who are likely to achieve maximum benefit from the PR programme is crucial. So far, several studies have shown that severe airflow limitation or poor exercise tolerance at baseline may predict a better response to PR [ 5 , 6 ], but another study has reported inconsistent findings [ 7 ]. Furthermore, one study reported that patients with severe dyspnoea did not respond well to PR and patients with milder dyspnoea responded well [ 8 ].

Considering the role of DLH in the development of dyspnoea and poor exercise tolerance in patients with COPD, objective measures that reflect the degree of DLH may help in identifying good responders to PR. Previously, we reported that there was an association between increased dyspnoea due to DLH on exercise and decreased exercise capacity in patients with COPD and reduced mobility of the diaphragm, which was assessed by the maximum level of diaphragm excursion (DE max ) using ultrasonography [ 9 ]. Other research groups reported the utility of ultrasonographic assessment of diaphragmatic mobility in COPD in understanding its association with 6-min walk distance (6MWD), dyspnoea [ 10 ] and increased mortality [ 11 ].

However, there have been no reports on the association between diaphragmatic mobility and the effect of PR to improve exercise tolerance. The primary aim of this study is to clarify the role of DE max to predict the improvement in exercise tolerance after PR in patients with COPD.

Materials and methods

Study design and subjects.

This was a single-centre, observational, prospective cohort study. The study included 62 patients with clinically stable COPD who visited the Department of Respiratory Medicine and Allergology, Kindai University Hospital, between April 2018 and February 2021. The exclusion criteria included unstable medical conditions that could cause or contribute to breathlessness, such as metabolic, cardiovascular or other respiratory diseases, or any other disorders that could interfere with exercise testing, such as neuromuscular diseases or musculoskeletal problems. This study was approved by the Ethics Committee of Kindai University School of Medicine. Written informed consent was obtained from all participants.

Measurements

All participants underwent ultrasonography (Xario 200, Toshiba, Tokyo, Japan) for the assessment of their DE max . Using the liver as an acoustic window (Fig.  1 A), a convex 3.5 MHz probe was used to measure the excursions of the right hemidiaphragm according to the techniques mentioned in previous studies [ 9 , 12 , 13 ]. The M-mode cursor was rotated and placed on the axis of diaphragmatic displacement on the stored image, and displacement measurements were performed. Measurements were performed during each of the three deep breaths, and DE max was measured (Fig.  1 B). The maximum value obtained for the three deep breaths was used. 6MWD was performed to evaluate walking capacity according to the American Thoracic Society (ATS)/European Respiratory Society (ERS) statement [ 14 , 15 , 16 ]. All participants performed the 6MWD test before and after the PR programme, and the magnitude of their perceived breathlessness and their leg fatigue was rated using a 1–10-point Borg scale. Responders to PR in exercise capacity were defined as those who demonstrated more than 30 m increase in 6MWD after the PR programme, which was the definition of minimal clinically important difference (MCID) for 6MWD [ 17 ].

Representative image of the right diaphragm. The probe was positioned below the right costal margin between the midclavicular and anterior axillary lines. A Two-dimensional ultrasonographic image of the right hemidiaphragm (B-mode). Diaphragmatic movements were recorded in M-mode during deep breathing (DE max ) ( B )

Spirometry (CHESTAC-800, Chest, Tokyo, Japan) was performed following the 2005 ATS/ERS recommendations [ 18 ] for measuring forced vital capacity (FVC), forced expiratory volume in 1 s (FEV 1 ) and inspiratory capacity. Respiratory muscle strength was assessed by measuring the maximum inspiratory pressure (PI max ) generated against an occluded airway at residual volume [ 19 ] (SP-370, Fukuda Denshi, Tokyo, Japan). A hand-held dynamometer (μTasF-1, Anima Corp., Tokyo) was used to measure quadriceps muscle strength (QMS). The impact of COPD on health status was assessed using the COPD assessment test (CAT), a patient-completed questionnaire on eight items, namely, cough, phlegm, chest tightness, breathlessness, limited activities, confidence leaving home, sleeplessness and energy. The scores for each of the items range from 0 to 5 points, resulting in a CAT total score ranging from 0 to 40 points [ 20 ], and MCID of CAT is 2 points [ 21 ]. In all patients with COPD, emphysema was evaluated by computed tomography of the chest. A SYNAPSE VINCENT volume analyser (FUJIFILM Medical, Tokyo, Japan) was used to measure the low attenuation area (%LAA).

Rehabilitation programme

The outpatient PR programme was conducted twice a week for 12 weeks (24 sessions), including aerobic exercise training (ergometer and walking exercise) at 60–70% of peak workload for 20–40 min and upper- and lower-limb muscle strength training for 10–20 min.

Sample size

The sample size was estimated using R software. The analysis based on 6MWD data from the PR programme revealed that 40 subjects were required if the expected area under the curve (AUC) below the receiver operating characteristic (ROC) curve was 0.80, the power was 90%, and the significance level was 0.01. Furthermore, we anticipated a dropout from the PR programme. Thus, we set the sample size to 50 participants.

Statistical analysis

Responders and non-responders were compared using t -test, the Wilcoxon rank-sum test or χ 2 test, as appropriate. The paired t -test or the Wilcoxon signed-rank test was used to evaluate the changes in the parameters before and after the PR programme. The Pearson correlation coefficient was used to analyse the relationship between changes in 6MWD and independent variables because changes in 6MWD were normally distributed. Additionally, multivariate logistic regression models were used to assess the ability of variables to predict a response to PR. The ROC curve method was used to assess the ability of DE max to predict a response to PR. All statistical analyses were performed using the JMP software programme (JMP®, Version 14; SAS Institute Inc., Cary, NC, USA).

Out of the 62 patients included in the study, 50 completed the PR programme (Fig.  2 ). Two patients dropped out because of severe exacerbation of COPD, and 10 patients discontinued the PR owing to the coronavirus pandemic. Table 1 presents the baseline characteristics of the participants. After the PR programme, scores for CAT, 6MWD, peak dyspnoea and leg fatigue of the modified Borg (mBorg) scale, and QMS improved significantly (Table 2 ). Thirty patients showed an increase of > 30 m in 6MWD after PR (responders: 60%), and 20 patients (40%) were defined as non-responders. Baseline levels of %FEV 1 , 6MWD, PI max , DE max and QMS were significantly higher and those of CAT score and peak dyspnoea of mBorg scale were significantly lower in responders than in non-responders (Table 1 ). Changes in 6MWD were significantly correlated with baseline levels of CAT, %FEV 1 , peak dyspnoea of mBorg scale, PI max , DE max (Fig.  3 ) and QMS and marginally correlated with baseline levels of 6MWD (Table 3 ).

Study flow diagram. COPD chronic obstructive pulmonary disease, PR pulmonary rehabilitation, 6MWD 6-min walk distance

Relationship between DE max and the changes in 6MWD after pulmonary rehabilitation. Changes in 6MWD were significantly positively correlated with DE max (r = 0.72; p < 0.001). DE max maximum diaphragmatic excursion, 6MWD 6-min walk distance

In multivariate analysis, DE max alone significantly contributed to the prediction of responders (Table 4 , Model 1). When using PI max instead of DE max because PI max and DE max showed a strong association (r = 0.73), both PI max and %FEV 1 contributed to the prediction (Table 4 , Model 2). The area under the ROC curve of DE max to predict the responders was 0.915, with a sensitivity of 83% and a specificity of 95% at a cut-off value of 44.9 mm of DE max (Fig.  4 ). The significance of DE max in the predictability of responders remained even when the analysis was confined to severe patients (%FEV 1  < 50%, n = 23; AUC = 0.88, sensitivity = 70% and specificity = 100% at a cut-off value of 44.9 mm).

Receiver operating characteristic (ROC) curve for baseline DE max in relation to the response to pulmonary rehabilitation. ROC curve estimates the ability of DE max to predict a clinically important improvement in 6MWD (> 30 m) after pulmonary rehabilitation (AUC = 0.915, sensitivity = 83% and specificity = 95% at a cut-off point of 44.9 mm of DE max ). AUC area under the curve, 6MWD 6-min walk distance, DE max maximum diaphragmatic excursion

This is the first study to demonstrate the utility of DE max to predict the responsiveness of patients with COPD to 12-week PR. In this study, multivariate analysis revealed that greater baseline DE max was the only factor that predicted the responsiveness to PR, independent of baseline %FEV 1 . Additionally, the model using DE max had better prediction performance than that using PI max . The AUC of DE max to predict the 30 m or more improvement in 6MWD after the PR was 0.915, with a sensitivity of 83% and a specificity of 95% at 44.9 mm.

PR is beneficial to patients with chronic respiratory disease, including COPD [ 3 ], and generally improves exercise performance, health-related quality of life and dyspnoea [ 22 ], which was confirmed in this study. Ideally, PR was proven to be effective in all patients, but the response to PR varies considerably between individual patients [ 8 , 23 , 24 , 25 ]. Indeed, in this study, the improvement in 6MWD was less than that in MCID in 40% of the patients regardless of the degree of severity of COPD. Therefore, identifying predictors of a response is crucial in ensuring better PR efficacy and personalisation of PR programmes for patients with COPD.

In this study, the baseline values of %FEV 1 , PI max , DE max , QMS and 6MWD were positively associated with Δ6MWD in univariate analysis, suggesting that a better baseline condition was associated with a higher proportion of patients who achieved MCID after PR. These findings are consistent with those of previous studies that showed that patients with higher levels of %FEV 1 or FEV 1 /VC achieved greater improvement in 6MWD after PR [ 7 , 26 , 27 ] and a study in which patients with milder mMRC scores could achieve MCID of 6MWD after PR [ 8 ], but not for those with worst mMRC score, although others studies showed contradictory results [ 5 , 6 , 28 , 29 , 30 ] or found no significant baseline characteristics to predict a response to PR [ 31 ]. The discrepancy between the findings cannot be fully explained, but it might be due to the differences in the studied population and strength or length of PR. In this study, the mean %FEV 1 of the participants was 56.0%, which was relatively higher than that of other studies (mean %FEV 1 of 40–50% in most studies) [ 5 , 6 , 28 ], despite similar inclusion criteria throughout the studies, i.e., not limited to severe COPD in most studies. Thus, no ceiling effect with a PR programme that included high-intensity load exercise training for 20–40 min was observed in our population.

In this study, an important finding is that greater DE max at baseline was the only factor that predicted the responders in 6MWD after PR. In addition, the model using DE max had better prediction performance than that using PI max . The high predictability of DE max may be because of its strong association with DLH and dyspnoea during exercise, as reported previously [ 9 ]. DLH is involved in the development of dyspnoea, and both are important factors to determine the improvement in 6MWD in patients with COPD. Therefore, DE max that reflects the degree of DLH and dyspnoea during exercise was superior to other physiological indices to predict responders.

Furthermore, the virtuous cycle observed in our PR programme that included high-intensity load exercise training might be a result of the improvement in ventilation pattern. Improving the ventilation pattern would be easier with greater DE max , as shown in studies of mechanically ventilated patients [ 32 ], which may have reduced dyspnoea during exercise after 12 weeks of PR and improved exercise tolerance. Exercise therapy is a central component of PR, which significantly reduces blood lactate levels during exercise, reduces minute ventilation and improves exercise tolerance [ 33 ]. The high-intensity load exercise training, which is performed at 60–80% of the maximum oxygen uptake, has a higher physiological effect than low exercise load. Patients with greater DE max may be able to perform higher load training, which resulted in effective PR.

Diaphragm ultrasonography has been widely and successfully used to identify diaphragmatic dysfunction by showing its association with 6MWD, dyspnoea [ 10 ], extubation failure in mechanically ventilated patients [ 32 ], and increased mortality [ 11 ]. Recently, Lewinska and Shahnazzaryan proposed its use in pulmonary physiotherapy of patients with COPD [ 34 ]. In most previous studies, diaphragm ultrasonography was used to assess DE max , i.e., the measurement of the excursion of the right hemidiaphragm, as used in this study, and diaphragm thickness that assessed the length and thickness of the zone of apposition of the diaphragm against the rib cage [ 35 , 36 ]. However, it is difficult to measure diaphragm thickness in patients with severe COPD because the length of the zone of apposition is shorter in patients with COPD than that in control subjects [ 37 ], whereas it is easy to measure DE max, which shows high intra- and inter-observer reliability [ 38 ]. Bhatt et al. showed that improvement in 6MWD was associated with that in DE max during forced expiration when the effectiveness of pursed lips breathing was assessed in the PR of patients with COPD [ 39 ]. Corbellini et al. demonstrated greater improvement in DE max during inspiration after PR, which was associated with an increase in the inspiratory capacity [ 40 ]. The normal and cut-off values of DE max during normal respiration, forced respiration, and voluntary sniffing have been described for each gender [ 38 ]. Thus, DE max would be a useful and reliable measure for incorporation into the PR assessment. Furthermore, in clinical settings, this objective measure of DE max has additional advantages as it requires minimum effort in patients and can be applied to the PR programme at home if portable ultrasonography is used. However, the assessment of DE max has a limitation. The procedures pertaining to positioning of patients, breathing patterns, and the selected hemidiaphragm are not standardised at present, which may hamper the routine use of DE max at this moment. Standardisation of these parameters would further facilitate the use of DE max in clinical settings and for research purpose.

There are some limitations to this study. This was a single-centre study involving a relatively small number of participants, and their baseline condition might have been relatively preserved. Nonetheless, 46% of the participants showed FEV 1  < 50%, and the utility of DE max was also observed in these patients with severe airflow limitation. Furthermore, in this study, few patients discontinued the PR programme, except for patients who discontinued during the coronavirus pandemic, which indicates that there was no severe mismatch between the PR programme and the patients’ ability to successfully complete this programme. As another limitation, we did not evaluate any malnutrition factors, which could be an important determinant of diaphragmatic mobility. Nonetheless, DE max was a stronger predictor of the effectiveness of PR than other parameters, including QMS or lung function using multivariate analysis. Further studies with a large number of patients are required, and the utility of DE max should be examined in patients with the most severe form of COPD with a low-intensity load exercise programme.

In conclusion, DE max , which is a reliable and easy to perform measurement, could adequately predict the improvement in exercise tolerance after PR in patients with COPD. Assessment of DE max could aid in making medical decisions associated with therapeutic strategies.

Availability of data and materials

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Abbreviations

Chronic obstructive pulmonary disease

Dynamic lung hyperinflation

• Pulmonary rehabilitation

6-Min walk distance

Minimal clinically important difference

Forced vital capacity

Forced expiratory volume in 1 s

Maximum inspiratory pressure

Quadriceps muscle strength

COPD assessment test

Low attenuation area

Area under the curve

Receiver operating characteristic

Modified Borg

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Acknowledgements

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This work was supported by Grants-in-Aid for Scientific Research (21K11325).

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Masashi Shiraishi, Yuji Higashimoto, Ryuji Sugiya, Hiroki Mizusawa, Yu Takeda, Shuhei Fujita, Tamotsu Kimura & Kanji Fukuda

Department of Respiratory Medicine and Allergology, Kindai University School of Medicine, Osaka, Japan

Masashi Shiraishi, Osamu Nishiyama, Yuji Tohda & Hisako Matsumoto

Inclusive Medical Science Research Institute, Morinomiya University of Medical Sciences, Osaka, Japan

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Contributions

MS, YH, and YC made substantial contributions to the conception and design of the work. MS, YH, and RS made substantial contributions to the data acquisition. MS and HM made substantial contributions to the analysis. All of the listed authors designed the study and were involved in the interpretation of the data. MS and HM drafted the work. YH, MS, TK, YC, ON, KS, KF, YT, and HM revised the report critically for important intellectual content. All authors approved the final version to be published and agreed to be accountable for all aspects of the work. All authors read and approved the final manuscript.

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Correspondence to Masashi Shiraishi .

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Shiraishi, M., Higashimoto, Y., Sugiya, R. et al. Diaphragmatic excursion is correlated with the improvement in exercise tolerance after pulmonary rehabilitation in patients with chronic obstructive pulmonary disease. Respir Res 22 , 271 (2021). https://doi.org/10.1186/s12931-021-01870-1

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• Diaphragmatic excursion
• Six-minute walk distance (6MWD)

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Clinical values of diaphragmatic movement in patients with chronic obstructive pulmonary disease

• Taehwa Kim 1 , 2   na1 ,
• Sungchul Huh 3   na1 ,
• Jae Heun Chung 1 , 2 ,
• Yun Seong Kim 1 , 2 ,
• Ra Yu Yun 3 , 4 ,
• Onyu Park 5 &
• Seung Eun Lee   ORCID: orcid.org/0000-0002-4266-7722 1 , 2  

BMC Pulmonary Medicine volume  23 , Article number:  33 ( 2023 ) Cite this article

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The limitation of activity due to dyspnea in chronic obstructive pulmonary disease (COPD) patients is affected by diaphragmatic dysfunction and reduced lung function. This study aimed to analyze the association between diaphragm function variables and forced expiratory volume in the first second (FEV1) and to estimate the clinical significance of diaphragm function in the correlation between COPD severity and lung function.

This prospective, single-center, cross-sectional observational study enrolled 60 COPD patients in a respiratory outpatient clinic. Data for baseline characteristics and the dyspnea scale were collected. Participants underwent a pulmonary function test (PFT), a 6-minute walk test (6MWT), and diaphragm function by ultrasonography.

The right excursion at forced breathing showed the most significant correlation with FEV1 ( r = 0.370, p = 0.004). The cutoff value was 6.7 cm of the right diaphragmatic excursion at forced breathing to identify the FEV1 above 50% group. In the group with a right diaphragmatic excursion at forced breathing < 6.7 cm, modified Medical Research Council (mMRC), St. George's Respiratory Questionnaire and the total distance of 6MWT showed no difference between groups with FEV1 under and above 50% ( p > 0.05). In the group with ≥ 6.7 cm, mMRC and the total distance of 6MWT showed a significant difference between FEV1 under and above 50% ( p = 0.014, 456.7 ± 69.7 m vs. 513.9 ± 60.3 m, p = 0.018, respectively).

The right diaphragmatic forced excursion was closely related to FEV1, and analysis according to the right diaphragmatic forced excursion-based cut-off value showed a significant difference between both groups. When the diaphragm function was maintained, there was a lot of difference in the 6MWT’s factors according to the FEV1 value. Our data suggest that diaphragmatic function should be performed when interpreting PFT.

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Introduction

The most common complaint in respiratory diseases regardless of the disease type is dyspnea [ 1 ]. COPD is characterized by worsening dyspnea during movement [ 2 ]. COPD restricts various activities of daily living due to shortness of breath, leading to poor quality of life and increased mortality and morbidity [ 3 ]. There are many causes of dyspnea; however, for patients with stable COPD, a major contributor is the weakening of the respiratory muscles, excluding conditions such as acute infectious diseases [ 4 ].

The diaphragm is the main respiratory muscle, particularly the inspiratory muscles. The weakness of the diaphragm in COPD has been extensively studied. Some studies have reported a significant reduction in diaphragmatic excursion in patients with COPD [ 5 , 6 , – 7 ]. Lung hyperinflation-associated shortening of the diaphragm has traditionally been considered a major cause of diaphragmatic weakness [ 8 ]. Also, there were previous studies about diaphragmatic thickness. Diaphragmatic thickness was a factor related to weaning and prognosis in patients under mechanical ventilation [ 9 , 10 ]. Recently, several studies have reported the clinical value of diaphragm ultrasonography according to COPD severity, and even compared to traditional methods, the diagnostic value of ultrasonography has proven to be reliable and useful [ 11 ]. Ultrasonography is also commonly used in medical facilities because it can be carried out anywhere, has no associated radiation risk, and can be used to adequately visualize the structure of the diaphragm [ 12 ].

Furthermore, 6MWT is an important tool for assessing exercise capacity and functional status in patients with COPD. Diaphragmatic weakness can impair physical performance, especially the 6MWT [ 13 , 14 ]. A previous study reported that pulmonary function was significantly correlated with the 6MWT in patients with severe and very severe COPD [ 15 ]. The relationship between 6MWT and PFT is a matter of connecting and understanding the respiratory muscles. PFT is used to measure the volume and flow rate of the lungs, and 6MWT is an important test for evaluating the exercise capacity and functional status of patients.

When we summarize the above, PFT correlates with 6MWT in COPD patients [ 15 ]. 6MWT can evaluate physical performance of COPD patients. Physical performance can also reflect diaphragmatic weakness [ 13 , 14 ]. Therefore, PFT correlates with 6MWT, 6MWT reflects physical performance, and physical performance was associated with diaphragmatic weakness. This relationship of PFT and diaphragmatic weakness can be expressed as follows for the patient. If the pulmonary function expressed by PFT is good, or if case which the power and strength of the respiratory muscles are good when PFT remains the same, breathing is more stable. Therefore, understanding the physiological principles of the respiratory muscle performance that establish the relationship these and compensate for this is important for managing the patient’s condition. Through this study, a review of the correlation between the PFT reflecting the 6MWT and diaphragm ultrasound features of respiratory muscle may be helpful to understand the physiological principles of patients with COPD.

Thus, this study aimed to analyze diaphragm movement characteristics using ultrasonography in patients with COPD and clarify its association with pulmonary function.

Study design and methods

Study design and participants.

This single-center, prospective, cross-sectional observational study recruited participants from a tertiary hospital outpatient respiratory clinic between April 2020 and April 2021. The inclusion criteria were: 1) patients 18 years old or older diagnosed with COPD by a pulmonologist; COPD diagnostic criterion was a post-bronchodilator FEV1/forced vital capacity (FVC) ratio < 0.70 based on the Global Initiative for Chronic Obstructive Lung Disease (GOLD), 2) patients who could maintain the required posture for diaphragm function measurement by ultrasonography and stable breathing during the examination such as 6MWT. Patients unable to cooperate with the examination and unstable patients requiring immediate medical intervention were excluded. Patients with interstitial lung disease featured on chest computed tomography (CT) that could affect diaphragm movement were also excluded.

Sixty-nine patients were enrolled, six of whom with combined interstitial lung disease on CT were excluded. Two patients were lost to follow-up, and one died before all examinations were completed. Finally, 60 patients completed all examinations for the study protocol and were included in the analysis.

All patients provided informed consent before participating in the study. Each patient’s clinical information was collected from four domains: pulmonary function, exercise capacity, body composition, and diaphragm function. Pulmonary function was evaluated through spirometry, MIP, and maximal expiratory pressure (MEP). Exercise capacity and body composition were assessed using the 6MWT and bioelectrical impedance analysis (BIA). Diaphragm dysfunction is defined as loss of muscle contractility [ 16 ]. To evaluated diaphragm dysfunction, we was assessed using ultrasonography in both the M-mode and B-mode for excursion and thickness, respectively.

Assessments

For patients who had performed a PFT within 1 month of participating in the study, the previous results were used and no retesting was performed. Patients who had no available PFT results within 1 month of participating in this study were reevaluated after enrollment. The Carefusion Vmax 20 (VIASYS Healthcare Inc. Sensormedics; Yorba Linda, CA, USA) was used for PFTs and FEV1, FVC, diffusing capacity of the lungs for CO, and total lung capacity were measured using the body plethysmography test. Regarding spirometry, the patients sat in a small booth and breathed into a mouthpiece. One technical expert from the Department of Respiratory Medicine conducted all the tests to maintain the consistency of the results.

MIP (PONY FX, COSMED Inc.; Rome, Italy) and MEP (PONY FX, COSMED Inc.; Rome, Italy) were measured in the sitting position using a portable mouth pressure meter. Three consecutive MIP and MEP measurements were taken, and the best result was recorded. The PFT was measured in a sitting position. A flanged mouthpiece was applied to the short and rigid tube of the measuring instrument and air leakage was checked around the mouthpiece before testing. The test was performed by an experienced examiner who has conducted the test for more than 8 years. MIP was measured by exhaling as deep as possible and inhaling as hard as possible for at least 1.5 s. MEP was measured by inhaling as deep as possible and exhaling as hard as possible for at least 1.5 s. Both measurements were made three times, and patients recovered to normal breathing patterns with at least a minute of break between measurements. The highest of the three measurements was recorded [ 17 ].

The 6MWT was performed according to the American Thoracic Society standards under the direction of a well-trained respiratory therapist at a 30 m indoor walking course [ 18 ]. Patients were encouraged by the instructor every minute and were allowed to rest or quit the test at any point. We measured the total distance and peripheral saturation with the portable oxygen meter. The patients’ body compositions were estimated indirectly using the BIA from a supine position (InBody S10, InBody, Co. Ltd., Seoul, Korea).

Diaphragm function was assessed using ultrasonography (LOGIQ E9, GE Healthcare; Chicago, IL, USA) obtained from both supine and sitting positions. It is generally accepted that there are positional differences in diaphragm contractility. The effects of gravitational loading on the diaphragm length-tension and body position-mediated changes in intra-abdominal pressure may explain the differences found. Not only that there is also a difference in the excursion between right and left. The excursion of the right diaphragm shows a lower value than that of the left diaphragm because the liver in the abdominal cavity restricts the movement of the right diaphragm. We also measured the diaphragm function in two positions based on this information. The supine position involved lying on the back or with the face upward while the sitting position was semi-seated (45–60 degrees). Both M-mode and B-mode imaging were used to evaluate diaphragmatic excursion and thickness, respectively. The mid-clavicular line and the liver were used as anatomical landmarks on the right side and the spleen on the left side to visualize the diaphragm in the M-mode. B-mode ultrasonography was used to measure the diaphragmatic thickness at the bilateral zone of apposition [ 19 ]. The diaphragm thickness was measured during quiet spontaneous breathing without peak inspiratory or expiratory maneuvers. The diaphragmatic thickness fraction was calculated as the difference between thickness at the end of inspiration and thickness at the end of expiration divided by thickness at the end of expiration x 100. The diaphragmatic excursion was measured as follows. The highest position of the diaphragm movement taken by the M-mode was considered to be the end-expiratory phase, whereas the lowest position was considered as the end-inspiratory phase.

The dyspnea scale used St. George's Respiratory Questionnaire (SGRQ) and the modified Medical Research Council scale (mMRC scale). The SGRQ is a self-administered questionnaire with 76 items [ 20 ]. This can identify the patient’s symptoms and the activities of daily life. mMRC scale is most commonly used in the assessment of dyspnea in chronic respiratory diseases and is a very useful and unrecognized dyspnea scale [ 21 ].

Statistical analysis

The data were analyzed using IBM SPSS (version 27.0; Chicago, IL, USA). The level of significance was set at p  < 0.05. Descriptive statistics, including numbers, percentages, means, and standard deviations, were used to summarize each variable (demographics, PFTs, 6MWT, and diaphragmatic ultrasound results). The results were analyzed by independent t-test, cross-analysis, and frequency analysis. The correlation between the variables was analyzed by Pearson’s Correlation Coefficient, which confirmed the linear relationship between two variables using a scatterplot. The cut-off value was calculated using the receiver operating characteristic (ROC) curve analysis. The reference plane was 0.5 or more in the ROC curve, and the p -value < 0.05; hence, this result was adopted. Consequently, the cut-off value was confirmed when sensitivity and specificity were plotted in a line chart, which is the point where the two graphs meet.

Ethics statement

We certify that all applicable institutional and governmental regulations concerning the ethical use of human volunteers were followed throughout this study. The study procedures were reviewed and approved by our Pusan National University Yangsan Hospital Institutional Review Board [IRB No. 05–2020-217].

FEV1 and diaphragm function

We assessed whether diaphragm function was associated with FEV1 (Fig.  1 ). In the total group analysis, both diaphragmatic excursion and thickness were associated with FEV1. However, the diaphragmatic excursion was more associated with FEV1 than thickness. Diaphragmatic excursion during forced breathing and in the supine position had a greater association with FEV1 than breathing at rest and in the sitting position. Additionally, when comparing the right and left under the same conditions, the right was more significant during forced breathing and in the supine position ( r =  0.370, p  = 0.004,). Moreover, diaphragmatic thickness at right end-expiration was associated with FEV1. In summary, right ( r =  0.370, p  = 0.004) and left ( r =  0.257, p  = 0.048) diaphragmatic excursion during forced breathing in the supine position and diaphragmatic thickness at right end-expiration ( r =  0.310, p  = 0.016) were significantly associated with FEV1.

Correlation between forced expiratory volume in 1 s and diaphragm function Right forced excursion, and left forced excursion in the supine position and right end-expiratory thickness were correlated to forced expiratory volume in 1 s

Diaphragmatic function and BMI (body mass index)

To evaluate the function of the diaphragm muscle [ 22 ], the diaphragmatic excursion was measured at rest and during forced expiration (Supplement Table  1 ). In 60 patients, diaphragmatic excursion at rest in the supine position was 3.5 cm ± 1.2 on the right side and 3.5 cm ± 1.2 on the left side. During forced breathing, diaphragmatic excursion in the supine position was 6.9 cm ± 2.0 on the right side and 7.6 cm ± 1.6 on the left side. The total percent body fat was 24.2% ± 6.9. Segmental lean mass analysis was performed by direct segmental multi-frequency BIA. The lean mass was 90.5% ± 9.7 on the right arm, 88.1% ± 9.2 on the left arm, 94.5% ± 5.8 on the trunk, 95.7% ± 131.3 on the right leg, and 9.51% ± 8.8 on the left leg.

Cutoff value-associated characteristics

The ROC curve analysis of the diaphragm function variables was performed to identify the cutoff value for differentiating between FEV1 ≥ 50% and < groups. The cutoff value was ≤ 6.7 cm on the right diaphragmatic excursion at forced breathing with an area under the curve of 0.5 or more and p -value was 0.043. Right diaphragmatic excursion during forced breathing was less than the cut-off value of 6.7 cm for 26 patients and ≥ 6.7 cm for 43 patients (Table  1 ). There were no differences in age, sex, or smoking history between the two groups. The dyspnea scales such as mMRC, SGRQ, and GOLD were not significantly different between both groups. There were no differences in body mass index, percent body fat, or lean mass of the right or left legs between the groups. However, among the pulmonary function indicators, there were significant differences between the two groups. Specifically, FEV1, FVC, and MIP were significantly different (< 6.7 cm group vs. ≥ 6.7 cm group, FEV1: 49.2% ± 16.2 vs. 59.5% ± 17.2, p  = 0.021; FVC: 76.2% ± 19.1 vs. 86.0% ± 15.5, p  = 0.032; MIP: 67.4 cm H 2 O ± 25.1 vs. 86.5 cm H 2 O ± 28.7, p  = 0.010). Concerning the 6MWT, there was a significant difference in SpO2 before 6MWT and the number of interruptions (SpO2 before 6MWT: 94.1% ± 2.7 vs. 95.3% ± 1.6, p  = 0.038; number of interruptions: 4 [15.4%] vs. 0 [0%], p  = 0.018). The left diaphragmatic excursion during forced breathing was also different between the two groups (6.8 cm ± 1.5 vs. 7.6 cm ± 1.3, p  = 0.022) as well as the diaphragmatic thickness during right end-inspiration (0.3 cm ± 0.1 vs. 0.4 cm ± 0.1, p  = 0.006). In addition, the ROC ≥ 6.7 cm group left diaphragmatic excursion was also measured with a value greater than that of the ROC < 6.7 cm group.

Subgroup characteristics according to FEV1

To identify the clinical significance of diaphragm function with the relationship between lung function, and COPD severity, the two groups classified as a right diaphragmatic excursion at 6.7 cm of forced breathing were further divided into groups based on FEV1 (< 50% or ≥ 50%) (Table  2 ). There were significant differences in age (65.0 ± 7.8 years vs. 72.7 ± 6.2 years, p  = 0.011), the GOLD score ( p  < 0.001), FEV1/FVC (40.1% ± 14.7 vs. 55.%4 ± 11.4, p  = 0.007), peak expiratory flow rate (183.3 L/min ± 80.4 vs. 275.8 L/min ± 113.8, p  = 0.027), SpO2 after the 6MWT (85.9% ± 6.5 vs. 91.5% ± 2.2, p  = 0.011), and left diaphragmatic excursion during forced breathing (6.2 cm ± 1.6 vs. 7.4 cm ± 1.0, p  = 0.038).

When the group with the right diaphragmatic excursion ≥ 6.7 cm was further divided into subgroups according to FEV1 (< 50% or ≥ 50%) and analyzed, mMRC, GOLD score, FEV1/FVC, MIP, peak expiratory flow rate, 6MWT, SpO2 before and after the 6MWT, and right diaphragmatic thickness at end-expiration subgroups were significantly different between the two groups.

This study contains the following: 1) evidence that FEV1 is significantly correlated with diaphragm movement, 2) cutoff values for diaphragm movement in patients with COPD, and 3) evidence to support the claim that the function of the diaphragm should be considered when interpreting the patient’s condition based on their FEV1.

First, FEV1 was significantly correlated with diaphragm movement. Studies on the relationship between the diaphragm and pulmonary function in patients with COPD are ongoing and have consistently reported that the severity of COPD and diaphragm function are closely related. Some previous studies have evaluated the direct relationship between FEV1 and diaphragm function [ 23 , 24 ].

The results of this study is also consistent with those of previous studies showing that diaphragm movement and FEV1 are related. However, beyond the findings of previous results [ 23 ], in our study, diaphragmatic excursion and thickness were found to be more correlated to FEV1 on the right side than on the left side.

Like the previous study that the thickness of the diaphragm is related to the ventilator weaning mechanical ventilation [ 9 , 10 ], this result has confirmed that the right diaphragm thickness was significantly related not only to the weaning of the ventilator and the prognosis of the patient but also to FEV1.

Second, we provided a cutoff value for a right diaphragmatic forced excursion in patients with COPD. Although there are studies that have presented a reference [ 23 ] value for healthy persons, the significant contribution of this study is the proposed reference value for patients with COPD.

We analyzed the correlation using Pearson’s correlation coefficient and confirmed the factors of diaphragmatic function-related components side (right, left), thickness, and excursion that were most-related to FEV1. Among them, Rt. forced excursion (supine), Lt. forced excursion (supine) and Rt. end-expiratory thickness showed meaningful p -value in association with FEV1. In addition, these three factors were analyzed in the linear relationship with the scattered plot and showed a proportional relationship between FEV1. Finally, when all factors related to the diaphragmatic function were analyzed, the right forced excursion was statistically determined as the most meaningful factor in relation to FEV1. We also obtained the cut-off value of 6.7 cm through the ROC curve.

The range in diaphragmatic excursion values varies considerably depending on the patient’s condition. A previous study has suggested normal values based on sex and the side of the diaphragm using healthy individuals. When breathing deeply, the right diaphragmatic excursion was 7 cm ± 1.1 in men and 5.7 cm ± 1 in women ( p  < 0.001) and the left diaphragmatic excursion were 7.5 cm ± 0.9 and 6.4 cm ± 1 in men and women, respectively ( p  < 0.01) [ 23 ]. In our study, we also assessed excursion during deep breathing to provide a cut-off value for patients with COPD.

When analyzed by dividing them into two groups based on a cut-off value, the following evaluation factors showed significant differences ( p  < 0.05): FEV1, FVC, MIP, left forced excursion, right diaphragmatic thickness during end-inspiration, 6MWT, the SpO2 before and after 6MWT, and interruption of the 6MWT.

These factors can be broadly divided into PFT-related and performance-related factors. As mentioned above, PFT-related factors such as MIP, left diaphragmatic forced excursion and right diaphragmatic thickness during end-inspiration were lower in the < 6.7 cm group. Moreover, the SpO2 level before the 6MWT was lower in the < 6.7 cm group, the overall 6MWT was shorter, and there were many interruptions in the 6MWT. These factors might reflect activity as a performance evaluation factor. Although generalizability is limited given the few patients and the fact that all the participants were outpatients who could walk; these results may reflect an actual patient’s status. However, these findings are intended for patients who can walk, suggesting that the cut-off value of 6.7 cm may be reliable in this population.

Finally, results concerning the degree of pulmonary function and correlations with the diaphragmatic movement were noteworthy. The two groups were analyzed based on the right diaphragmatic forced excursion (6.7 cm) and divided into subgroups based on FEV1 (< 50% vs. ≥ 50%). As a result, in the group that had maintained diaphragm function (≥ 6.7 cm), the MIP, portable peak flow meter, 6MWT, SpO2 before and after the 6MWT, and right diaphragmatic thickness at end-expiration were different between the two FEV1 groups. In summary, the difference between the two FEV1 groups was large when diaphragm function was maintained; when it was not maintained, there were no differences between the two FEV1 groups. Therefore, even in patients who maintained their FEV1 > 50%, when diaphragm function deteriorated, the patient’s 6MWT, SpO2 before and after the 6MWT were less predictable (they either deteriorated or were maintained). The patients whose FEV1 decreased < 50%, if the diaphragm function was maintained, the 6MWT could be better than that in patients with an FEV1 ≥ 50% and a reduced diaphragm function.

In conclusion, when interpreting a patient’s condition based on FEV1, it is important to assess diaphragm function, since the effect of the FEV1 value on the patient depends on how well the diaphragm function has been maintained.

In this study, when the diaphragm function was maintained, there were significant differences in MIP, peak expiratory flow rate, 6MWT, SpO2 before and after the 6MWT, and right diaphragmatic thickness at end-expiration according to FEV1 in patients with COPD. Even if the diaphragm function was not maintained, because there are still differences in the FEV1, it may be beneficial to consider diaphragmatic function measured by right diaphragm excursion as an additional indicator of function beyond the FEV1. Therefore, it can be clinically helpful to check whether the diaphragm is functioning properly when determining a patient’s condition based on FEV1.

Availability of data and materials

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Abbreviations

Chronic obstructive pulmonary disease

Pulmonary function test

• 6-minute walk test

Forced expiratory volume in the first second

Maximal inspiratory pressure

International Classification of Diseases 11TH

Forced vital capacity

Global Initiative for Chronic Obstructive Lung Disease

Computed tomography

Maximal expiratory pressure

Bioelectrical impedance analysis

Modified Medical Research Council

Receiver operating characteristic

Body mass index

St. George's Respiratory Questionnaire

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Acknowledgements

Abstract has been published/presented in the Korean tuberculosis and respiratory society, the Korean tuberculosis and respiratory society fall academic presentation | 129 volume 0342 ~ 343, total 2 PAGES, 2021

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This study was supported by the Research Institute for Convergence of Biomedical Science and Technology (30–2020-003), Pusan National University Yangsan Hospital. The funding body played no role in the design of the study and collection, analysis, and interpretation of data and in writing the manuscript.

Author information

Taehwa Kim and Sungchul Huh contributed equally to this work.

Authors and Affiliations

Division of Respiratory, Allergy and Critical Care Medicine, Department of Internal Medicine, Pusan National University Yangsan Hospital and Pusan National University School of Medicine, Geumo-ro 20, Beomeo-ri, Yangsan-si, Gyeongsangnam-do, 50612, Republic of Korea

Taehwa Kim, Jae Heun Chung, Yun Seong Kim & Seung Eun Lee

BioMedical Research Institute for Convergence of Biomedical Science and Technology, Pusan National University Yangsan Hospital, Yangsan, South Korea

Department of Rehabilitation Medicine, Rehabilitation Hospital, Pusan National University Yangsan, Yangsan, South Korea

Sungchul Huh & Ra Yu Yun

Pusan National University School of Medicine, Yangsan, South Korea

College of Nursing, Pusan National University, Pusan National University Yangsan Hospital, Yangsan, South Korea

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Conceptualization: TK, SEL. Data acquisition and analysis: TK, OP, RYY, SH, JHC, SEL. Data interpretation: TK, RYY, SH, JHC, SEL. Validation: TK, JHC. Writing – original draft: SH, TK. Writing – review: SEL, JHC, YSK. The author(s) read and approved the final manuscript.

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Kim, T., Huh, S., Chung, J.H. et al. Clinical values of diaphragmatic movement in patients with chronic obstructive pulmonary disease. BMC Pulm Med 23 , 33 (2023). https://doi.org/10.1186/s12890-022-02220-7

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Relationship Between Diaphragm Thickness, Thickening Fraction, Dome Excursion, and Respiratory Pressures in Healthy Subjects: An Ultrasound Study

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• Volume 202 , pages 171–178, ( 2024 )

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• Toru Yamada   ORCID: orcid.org/0000-0003-4583-364X 1 ,
• Taro Minami   ORCID: orcid.org/0000-0001-7373-939X 2 , 3 ,
• Shumpei Yoshino 4 ,
• Ken Emoto 5 ,
• Suguru Mabuchi   ORCID: orcid.org/0000-0002-8620-5191 1 ,
• Ryoichi Hanazawa   ORCID: orcid.org/0000-0002-4230-7356 6 ,
• Akihiro Hirakawa   ORCID: orcid.org/0000-0003-2580-7460 6 &
• Masayoshi Hashimoto 1  

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Diaphragm ultrasonography is used to identify causes of diaphragm dysfunction. However, its correlation with pulmonary function tests, including maximal inspiratory (MIP) and expiratory pressures (MEP), remains unclear. This study investigated this relationship by measuring diaphragm thickness, thickening fraction (TF), and excursion (DE) using ultrasonography, and their relationship to MIP and MEP. It also examined the influence of age, sex, height, and BMI on these measures.

We recruited healthy Japanese volunteers and conducted pulmonary function tests and diaphragm ultrasonography in a seated position. Diaphragm ultrasonography was performed during quiet breathing (QB) and deep breathing (DB) to measure the diaphragm thickness, TF, and DE. A multivariate analysis was conducted, adjusting for age, sex, height, and BMI.

Between March 2022 and January 2023, 109 individuals (56 males) were included from three facilities. The mean (standard deviation) MIP and MEP [cmH2O] were 72.2 (24.6) and 96.9 (35.8), respectively. Thickness [mm] at the end of expiration was 1.7 (0.4), TF [%] was 50.0 (25.9) during QB and 110.7 (44.3) during DB, and DE [cm] was 1.7 (0.6) during QB and 4.4 (1.4) during DB. Multivariate analysis revealed that only DE (DB) had a statistically significant relationship with MIP and MEP ( p  = 0.021, p  = 0.008). Sex, age, and BMI had a statistically significant influence on relationships between DE (DB) and MIP ( p  = 0.008, 0.048, and < 0.001, respectively).

In healthy adults, DE (DB) has a relationship with MIP and MEP. Sex, age, and BMI, but not height, are influencing factors on this relationship.

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Diaphragm Ultrasonography: Reference Values and Influencing Factors for Thickness, Thickening Fraction, and Excursion in the Seated Position

Assessment of diaphragmatic mobility by chest ultrasound in relation to BMI and spirometric parameters

Influence of gender on diaphragm thickness using a method for determining intima media thickness in healthy young adults

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Introduction

The diaphragm is the primary muscle involved in respiration. The diaphragm dysfunction is associated with exertional dyspnea, orthopneic breathing, reduced cough strength leading to aspiration risk, and difficulty in weaning from mechanical ventilation [ 1 , 2 ]. Diaphragm ultrasonography is a non-invasive and convenient method to assess diaphragm function and is useful in diagnosing diaphragmatic paralysis and predicting successful weaning from mechanical ventilation [ 1 , 2 ]. There are two measurement techniques: one measures the diaphragm excursion (DE) and the other evaluates diaphragm thickness and the change in thickness during respiration (thickening fraction: TF). Common diagnostic criteria for diaphragmatic paralysis include a thickness < 2 mm or a TF < 20% during deep breathing (DB) [ 1 , 3 , 4 ]. Furthermore, DE < 2 cm during quiet breathing (QB) has been proposed as a criterion for diaphragm dysfunction [ 5 ].

Diaphragm ultrasonography is becoming increasingly prevalent in clinical practice. Although diaphragm function might be closely related to respiratory function, the specific relationship between respiratory function tests and diaphragm ultrasonography has not been well established [ 6 , 7 , 8 ]. For instance, some studies suggested a relationship between thickness at functional residual capacity (FRC) and maximal inspiratory pressure (MIP), whereas others did not [ 6 , 9 , 10 , 11 ]. Similarly, results are mixed regarding the relationship between DE and maximal expiratory pressure (MEP) or MIP [ 6 , 12 , 13 , 14 , 15 , 16 ]. However, these studies had a small sample size. The populations vary between healthy individuals and patients with underlying conditions such as chronic obstructive pulmonary disease or head trauma, making it challenging to integrate the results. A recent systematic review of the relationship between diaphragm ultrasonography and respiratory function tests noted high heterogeneity in terms of study design [ 7 ]. Therefore, there is a need for standardized large-scale studies focusing on healthy individuals.

In this study, we conducted pulmonary function tests and diaphragm ultrasonography on 109 healthy Japanese volunteers to investigate the relationship between diaphragm ultrasonography parameters, including thickness, TF, and DE, with the MIP and MEP. Additionally, we explored factors that influenced these relationships.

Study Population and Setting

This study was a secondary analysis of a cross-sectional study of diaphragmatic ultrasonography on healthy Japanese [ 17 ]. Healthy adult Japanese volunteers, age 18-year-old or older, were recruited from three facilities in Tokyo, Fukuoka and Kanagawa prefecture. The recruitment period was from March 2022 to January 2023. On the examination day, volunteers provided information about their age, sex, height, weight, smoking history, and medical history. Subsequently, pulmonary function tests were conducted using a Spirometer (AutoSpiro507, Minato Medical Science Co. Ltd.) to measure the percent vital capacity (%VC), forced expiratory volume in one second (FEV1), and forced vital capacity (FVC). Only asymptomatic individuals with %VC ≥ 80% and FEV1/FVC ≥ 70% were included. MIP and MEP were measured twice each, and the better of the two results was used. All diaphragm ultrasonography measurements were performed by physicians certified as instructors in the Point of Care Ultrasound Simulation Course and by trained ultrasonography technicians.

Ultrasound Measurements of the Diaphragm

The right hemidiaphragm was measured by ultrasonography in a seated position. The DE of the right hemidiaphragm was assessed at the area around the eighth to ninth intercostal space along the anterior to mid-axillary line, where the diaphragm dome is visualized. A phased-array transducer (2.5 MHz) was placed longitudinally and perpendicularly to the chest wall and adjusted to avoid the ribs. The M-mode interrogation line was adjusted to be as perpendicular to the diaphragm as possible, and the difference in the dome’s movement during inspiration and expiration was measured. For the thickness of the right hemidiaphragm measurement, a linear transducer (7.0 MHz) was positioned longitudinally and perpendicularly at the zone of apposition of the diaphragm, near the eighth to ninth intercostal space along the anterior to mid-axillary line. It was then adjusted to avoid the ribs and positioned so that the lung was partially visible at the edge of the screen during inspiration. At this site, the diaphragm thickness during inspiration and expiration was measured. The thickness measurements were conducted in B-mode, with measurement markers placed from the center of the white line on the thoracic side of the diaphragm to the center of the white line on the peritoneal side. The TF was calculated as follows: (thickness at the end of inspiration − thickness at the end of expiration)/thickness at the end of expiration × 100. The TF and DE were measured during QB and DB.

Statistical Analysis

The patients’ characteristics, diaphragm thickness, TF, and DE are presented as the mean and standard deviation (SD) for continuous data and as counts and proportion for categorical data. Simple and multiple linear regression analyses were used to evaluate the associations between thickness, TF, and DE, and MIP and MEP. In the multiple linear regression analyses, patients’ characteristics including age, sex, height, and BMI were adjusted. We considered p  < 0.05 to indicate statistical significance. All data analyses were performed using STATA version 17.0 (StataCorp LLC, College Station, TX, USA).

Participants

A total of 111 Japanese volunteers were recruited for this study. Of these, two individuals were excluded because their %VC was below 80%, resulting in 109 participants being included. The proportion of male volunteers was 51%, with an average age of 31.8 years, ranging from 19 to 60 years. The average BMI was 22.5 for males and 21.7 for females, which was closely aligned with the Japanese national averages of 23.6 for males and 21.8 for females [ 18 ]. Two participants had a history of bronchial asthma but were asymptomatic on the day of measurement and had %VC and FEV1/FVC within the normal range. Patient characteristics are presented in Table  1 .

Diaphragm Thickness, TF, and DE

The mean values of measurements for the diaphragm thickness (FRC), TF (QB), TF (DB), DE (QB), and DE (DB) were 1.7 mm (SD 0.4), 50.0% (SD 25.9), 110.7% (SD 44.3), 1.7 cm (SD 0.6), and 4.4 cm (SD 1.4), respectively. The thickness and TF were measured in all participants during QB and DB. DE could not be measured in one individual during QB and in 10 individuals during DB because the lung overlaid the diaphragm during inspiration. The measurement results are presented in Table  2 .

Simple and Multiple Regression Analyses

Initially, a linear univariate regression analysis was conducted with MIP or MEP as the outcome variable to examine their relationship with diaphragm thickness, TF, and DE. A statistically significant relationship was observed between the MIP and DE during DB ( p  < 0.001), between the MEP and TF during QB ( p  = 0.048), and the DE during DB ( p  < 0.001). No relationship was found between the MIP or MEP, and thickness or TF during DB or DE during QB (Table  3 ).

In the multivariate linear regression analysis adjusted for age, sex, height, and BMI, a statistically significant relationship was only observed for DE during DB for the MIP ( p  = 0.008) and MEP ( p  = 0.021). Sex and BMI were statistically significant influencing factors for all parameters in relation to the MIP and MEP. Age had a significant influence on all parameters in relation to the MIP and MEP except for thickness and DE during DB for MEP. Height had no influence on any of the parameters (Table  4 and 5 ).

This study investigated the relationship between ultrasonographic findings (diaphragm thickness, TF, and DE) and pulmonary function test findings (MIP and MEP) in healthy volunteers. Additionally, it explored which factors influenced these relationships. This represents the largest-scale study to date conducted on a healthy population. [ 6 , 7 , 9 , 10 , 11 ] Results from the multiple regression analysis, adjusted for age, sex, height, and BMI, demonstrated a statistically significant relationship between the DE (DB), and the MIP and MEP. Thickness, TF (QB), and TF (DB) had no relationship with MIP and MEP. Although previous studies reported a relationship between the thickness, TF, and DE with MIP and MEP in healthy individuals, all were univariate analyses, and none had been adjusted for variables such as age, sex, or BMI [ 6 , 11 , 19 ]. However, previous studies reported relationships between the diaphragm thickness, TF, and DE with age, sex, and BMI [ 4 , 6 , 20 , 21 , 22 , 23 ]. To accurately evaluate the relationship between various diaphragm ultrasonography parameters and the MIP or MEP, it is essential to adjust for these factors. In this study, the univariate analysis indicated a relationship between the TF (QB) and MEP, although it was not observed in the multivariate analysis. Sex and BMI were statistically significant influencing factors in the relationship between thickness, TF, and DE, and MIP and MEP, with female sex having a negative influence and BMI a positive influence. Therefore, future studies that compare results between groups with significantly different average BMIs, such as Asians and Western populations, must consider the background BMI in their assessments.

Ultrasonographic Findings and MIP

In the current study, no relationship was found between the thickness (FRC) and MIP. This finding is consistent with previous studies involving 13 healthy individuals [ 11 ] and 64 healthy individuals [ 6 ]. Although these studies had small sample sizes, our analysis with 109 subjects also did not demonstrate a relationship between the thickness (FRC) and MIP. Two other studies that reported there was a relationship between the thickness (FRC) and MIP had sample sizes of 36 and 24 participants, respectively. Thus, our study sample size of 109 subjects can be considered sufficiently large in comparison [ 9 , 10 ]. Therefore, it is unlikely that the reason our study did not show a statistically significant relationship is due to an insufficient sample size. The first study included 36 participants, of whom 15 were weight-lifters and 3 were children [ 9 ] and the second study focused exclusively on 24 individuals aged 65 years and over [ 10 ]. Thus, the participant profiles in these studies were not representative of a general healthy population. In our findings, age had a negative influence and BMI had a positive influence on the variables ( p  = 0.033, p  < 0.001). Considering these facts, the two previous studies did not adjust for BMI when assessing the thickness of the diaphragm in weightlifters, who are presumed to have a thicker diaphragm than the general population, nor did they adjust for age when considering the elderly, who are presumed to have a thinner diaphragm, potentially affecting the outcomes [ 9 , 10 ]. Although thickness (FRC) might be an indirect indicator of muscle mass, this might not directly reflect muscle strength. Therefore, diaphragm thickness may not be directly applicable for predicting respiratory muscle strength [ 6 , 24 ].

TF, either in QB or DB, had no relationship with MIP. Few studies have examined the relationship between TF and MIP in healthy individuals. A study of 10 children with an average age of 11 years by Ho et al. reported a Spearman’s rank relationship coefficient of 0.64 between the TF and MIP [ 19 ]. In our multiple regression analysis, age had a negative influence on the relationship between TF and MIP. Because the results of the study by Ho et al. were not adjusted for age, it is possible that age had a significant impact on the study findings. However, it is unclear whether children and adults can be discussed in a similar fashion. Additionally, a study by Cardenas et al. [ 6 ], involving 64 healthy individuals, reported a positive relationship between the TF (DB) and MIP. The average BMI was 26.1 for males and 25.5 for females, which is higher than our study (22.5 for males and 21.7 for females). BMI had a positive effect on the relationship between TF and MIP in our result. However, the study by Cardenas did not adjust for BMI when performing the analysis, which might have influenced their results because the higher BMI in their study might have suggested a relationship between TF and MIP.

DE (DB) had a significant relationship with the MIP ( p  = 0.008), whereas DE (QB) did not ( p  = 0.408). These results are consistent with past studies [ 6 , 12 , 15 ]. However, a study by Dos Santos Yamaguti et al. reported the DE (DB) did not correlate with MIP [ 14 ]. That study targeted chronic obstructive pulmonary disease patients, who, compared with healthy individuals, had a markedly reduced DE, which might have influenced the results [ 14 ]. DE is a critical factor involved in altering thoracic content volume. A larger DE results in a greater change in thoracic content volume, thereby increasing the negative pressure on the lungs. Consequently, this can lead to an increase in MIP. The lack of a relationship between DE (QB) and MIP and the observed relationship with DE (DB) can be understood from this pathophysiological perspective.

Ultrasonographic Findings and MEP

No relationships were found between the thickness, TF (QB), TF (DB), DE (QB), and MEP. Given that the diaphragm is primarily involved in inspiration, it is plausible that it does not have a relationship with MEP. However, a significant relationship was observed between the DE (DB) and MEP. The reason for this may be the influence of the MIP and MEP being related. Simple regression analysis and multiple regression analysis adjusted for age, sex, height, and BMI showed a statistically significant positive relationship between the MIP and MEP (both p  < 0.001) (Supplementary Information 1 ). These findings might have impacted the observed relationship between the DE (DB) and MEP.

In light of these findings, diaphragmatic ultrasonography could be applied to predict successful weaning from mechanical ventilation. In fact, diaphragm ultrasonography has been used increasingly in intensive care units to predict successful weaning from mechanical ventilation [ 2 , 25 ]. This involves diaphragmatic ultrasonography during a spontaneous breathing trial (SBT) to assess the TF or DE, and to predict successful weaning. The combined sensitivity and specificity for DE are 0.85 and 0.75 whereas these values are 0.80 and 0.80 for TF during QB [ 2 ]. MIP and MEP are also important indicators of successful weaning [ 26 , 27 , 28 ], but measuring these in mechanically ventilated patients during routine clinical SBT is challenging. For instance, encouraging patients who are able to communicate to take deep breaths during SBT and evaluating the DE during DB may further increase the success rate of weaning. However, the threshold values for this are unknown, necessitating further research.

This study had some limitations. Because the participants in this study had an average BMI, it is unclear whether these results are applicable to patients with severe obesity. In cases of extremely high BMI, MIP may actually decrease because of factors such as reduced thoracic compliance. Additionally, since the subjects of this study are young, healthy individuals, it is unclear whether the findings can be applied to patients with underlying diseases or to the elderly. Further research is needed in the future.

In summary, this study investigated the relationship between ultrasonographic findings (diaphragm thickness, TF, and DE) and pulmonary function test findings (MIP and MEP) in healthy volunteers. The influence of age, sex, height, and BMI on these factors were also investigated. The DE (DB) was related to the MIP and MEP, whereas thickness (FRC), TF (QB), and TF (DB) had no relationship. Female sex and older age negatively influence the relationship. Higher BMI positively influences, whereas height does not have an influence.

Abbreviations

Body mass index

Deep breathing

Diaphragm excursion

Forced expiratory volume in one second

Functional residual capacity

Forced vital capacity

• Maximal expiratory pressure
• Maximal inspiratory pressure

Quiet breathing

Spontaneous breathing trial

Standard deviation

Thickening fraction

Total lung capacity

Percent vital capacity

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Acknowledgements

The authors are grateful to Heita Nakayama, Hiroshi Imura, Hiroyuki Ide, Megumi Honda, Namie Hattori, Riko Oda, Sachio Muramatsu, Takuya Tobari, and Yosuke Matsuzaki for their efforts in data collection and management of the research environment. This work was supported by JSPS KAKENHI Grant (Number JP20K16543). The authors thank J. Ludovic Croxford, PhD, from Edanz ( https://jp.edanz.com/ac ) for editing a draft of this manuscript.

This work was supported by JSPS KAKENHI Grant (Number JP20K16543).

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Toru Yamada, Suguru Mabuchi & Masayoshi Hashimoto

Medicine, Division of Pulmonary, Critical Care, and Sleep Medicine, The Warren Alpert Medical School of Brown University, Providence, RI, 02903, USA

Taro Minami

Medicine, Division of Pulmonary, Critical Care, and Sleep Medicine, Care New England Health System, Providence, RI, 02906, USA

General Internal Medicine, Iizuka Hospital, Iizuka, Fukuoka, 135-0041, Japan

Shumpei Yoshino

General Internal Medicine, Kaita Hospital, Iizuka, Fukuoka, 820-1114, Japan

Department of Clinical Biostatistics, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Bunkyo-ku, Tokyo, 113-8510, Japan

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Contributions

Toru Yamada, Taro Minami, Syumpei Yoshino, Ken Emoto, Suguru Mabuchi, and Masayoshi Hashimoto contributed to the design of the study. Toru Yamada, Syumpei Yoshino, Ken Emoto, and Suguru Mabuchi contributed to the data collection. The data were analyzed and interpreted by Toru Yamada, Ryoichi Hanazawa, and Akihiro Hirakawa. Toru Yamada, Taro Minami, and Masayoshi Hashimoto supervised the study. Toru Yamada wrote the first draft with input from Taro Minami. All authors contributed to the writing and review of the main manuscript, had full access to all the data in the study, and had final responsibility for the decision to submit for publication.

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Correspondence to Toru Yamada .

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Taro Minami is a consultant for FUJIFILM and AA Health Dynamics in relation to a project funded by the Ministry of Economy, Trade and Industry, Japan.

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The study was conducted in accordance with the Declaration of Helsinki and approved by the Institutional Review Board of Tokyo Medical and Dental University (protocol code M2020-112, date of approval: December 21th, 2021).

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Yamada, T., Minami, T., Yoshino, S. et al. Relationship Between Diaphragm Thickness, Thickening Fraction, Dome Excursion, and Respiratory Pressures in Healthy Subjects: An Ultrasound Study. Lung 202 , 171–178 (2024). https://doi.org/10.1007/s00408-024-00686-2

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DOI : https://doi.org/10.1007/s00408-024-00686-2

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† Massachusetts General Hospital, Department of Emergency Medicine, Boston, Massachusetts

Andrew J. Goldsmith

‡ Brigham and Women’s Hospital, Department of Emergency Medicine, Boston, Massachusetts

Joseph Brown

§ University of Colorado, Department of Emergency Medicine, Aurora, Colorado

Nicole M. Duggan

Arun nagdev.

Pain scales are often used in peripheral nerve block studies but are problematic due to their subjective nature. Ultrasound-measured diaphragmatic excursion is an easily learned technique that could provide a much-needed objective measure of pain control over time with serial measurements.

Case Series

We describe three cases where diaphragmatic excursion was used as an objective measure of decreased pain and improved respiratory function after serratus anterior plane block in emergency department patients with anterior or lateral rib fractures.

Diaphragmatic excursion may be an ideal alternative to pain scores to evaluate serratus anterior plane block efficacy. More data will be needed to determine whether this technique can be applied to other ultrasound-guided nerve blocks.

• INTRODUCTION

Peripheral nerve blocks are an important component of multimodal analgesia for thoracic pain. 1 The serratus anterior plane block (SAPB) involves placing local anesthetic into the fascial plane between the serratus anterior and latissimus dorsi muscles, or between serratus anterior and an underlying rib, using real-time ultrasound guidance. 2 Serratus anterior plane block can be used in a variety of settings including after surgery involving the chest wall or in the emergency care setting for anterior and/or lateral rib fractures. Rib fractures occur in 9–10% of all trauma patients. Controlling chest wall pain in these patients is crucial as inadequately treated pain is associated with increased risk of chest wall splinting leading to hypoventilation, atelectasis and, eventually, pneumonia. 3 , 4 Diaphragmatic excursion has been proposed as a surrogate objective method of respiratory status in this patient subpopulation. 5

Point-of-care ultrasound (POCUS) evaluation of diaphragmatic excursion can provide the quantification of diaphragmatic function over time through serial evaluation, and it has high sensitivity and specificity compared to chest radiography. 5 – 7 Further, diaphragmatic dysfunction can be caused by a variety of interventions and diseases including mechanical ventilation, cardiac and abdominal surgery, phrenic nerve injury, neuromuscular disorders, lung hyperinflation, and multi-organ dysfunction in critical illness. 8 Several reviews describing POCUS uses and techniques to evaluate the diaphragm have been published. 9 – 11

Specifically, diaphragmatic excursion may provide a quantification method of respiratory status after intervention. As visual pain scores are a subjective perception of an individual’s pain, objectively comparing this measurement has been a challenge in peripheral nerve block studies. 12 The excursion of the dome of the diaphragm can be used to guide clinicians on the degree of respiratory compromise in specific pulmonary pathologies. 13 , 14 As splinting secondary to rib fractures is a known phenomenon, diaphragmatic ultrasound may provide an objective outcome of successful nerve blocks for rib fractures. We propose diaphragmatic excursion as a new objective outcome of block efficacy in thoracic nerve blocks. Here we describe three cases where diaphragmatic excursion was used as an objective measure of SAPB efficacy in emergency department (ED) patients with anterior or lateral rib fractures.

To measure diaphragmatic excursion the patient is first placed in a supine position. A curvilinear probe is placed in the midaxillary line and oriented cephalad to optimally visualize the inferior aspect of the lungs, diaphragm, and upper abdomen (ie, spleen or liver). Diaphragmatic excursion was quantified on M-mode imaging, with the M-mode cursor directed through the diaphragm. The amplitude of diaphragmatic excursion was measured from the baseline to the point of maximal excursion on the vertical axis ( Image 1 ).

Diaphragmatic excursion is calculated by first determining a baseline (line a) and then measuring the distance of maximal vertical excursion (distance b).

Nagdev et al provide a complete description of SAPB. 15 In summary, the patient is placed in a lateral decubitus or supine position. A high-frequency linear transducer is placed in the midaxillary line at the level of the nipple to locate the serratus anterior muscle. A blunt-tip block needle is then used to inject anesthetic into the plane between the serratus anterior muscle and latissimus dorsi muscles. To perform the block, the needle is visualized using an in-plane approach until the tip is located just above the serratus anterior muscle. Once the correct position is confirmed, a large volume of anesthetic is injected into the fascial layer. As with all blocks, intralipid should be readily available in the event of local-anesthetic systemic toxicity syndrome.

CPC-EM Capsule

What do we already know about this clinical entity?

Pain scales are often used to measure the efficacy of peripheral nerve blocks but are problematic due to their subjective nature .

What makes this presentation of disease reportable?

This is the first description of diaphragmatic excursion as an objective measure of appropriate pain control in acute rib fractures in the emergency care setting .

What is the major learning point?

Diaphragmatic excursion is a promising novel tool to quantify improved pain and respiratory function after serratus anterior nerve block and possibly other blocks .

How might this improve emergency medicine practice?

This technique could be utilized in future studies of nerve block efficacy as well as clinically to guide appropriate pain control .

• CASE SERIES

A 44-year-old man presented after a motorcycle collision and was found to have right-sided fractures of ribs 2–5 and 12 on computed tomography (CT). The patient continued to report severe pain after 100 micrograms (mcg) of intravenous (IV) fentanyl. M-mode of the right diaphragm was performed prior to SAPB and showed 5 millimeters (mm) of diaphragmatic excursion and a respiratory rate of 24 breaths per minute (BPM) ( Image 2A ). A right ultrasound-guided SAPB was performed with 20 milliliters (mL) of 1% ropivacaine. On re-evaluation approximately 60 minutes later, M-mode of the right diaphragm showed a respiratory rate of 16 BPM and 14 mm of diaphragmatic excursion (increase of 64%) ( Image 2B ). Increase in diaphragmatic excursion was calculated as the change in diaphragmatic excursion (14 mm minus 5 mm) divided by the post-block diaphragmatic excursion (14 mm).

(A) Pre-block demonstrating right-sided diaphragmatic excursion of 5 millimeters (mm) (average of two excursions). (B) Post-block demonstrating right-sided diaphragmatic excursion of 14 mm (increase of 64%).

A 35-year-old man presented after an assault and was found to have a left lateral sixth rib fracture on CT. The patient received 1000 milligrams (mg) of IV acetaminophen but continued to report severe pain. M-mode of the left diaphragm was performed prior to SAPB and showed 8 mm of diaphragmatic excursion and a respiratory rate of 20 BPM ( Image 3A ). A left ultrasound-guided SAPB was performed with 20 mL of 1% ropivacaine. On re-evaluation approximately 60 minutes later, M-mode of the left diaphragm showed 17 mm of diaphragmatic excursion (increase of 53%) and a respiratory rate of 16 BPM ( Image 3B ).

(A) Pre-block demonstrating left-sided diaphragmatic excursion of 8 mm (average of three excursions). (B) Post-block demonstrating left-sided diaphragmatic excursion of 17 mm (increase of 53%).

A 50-year-old man presented with left-sided chest wall pain after a fall four days prior when intoxicated and was found to have fractures of ribs 6–9 on CT. The patient initially rated his pain 10/10 and was given 100 mcg of IV fentanyl. Pain continued to be 10/10 and a SAPB was performed for pain control. A left ultrasound-guided SAPB was performed with 20 mL of 0.5% bupivacaine combined with 10 mg of dexamethasone. The patient’s pain 60 minutes after the block was 2/10. A diaphragmatic POCUS was performed both before and 60 minutes after the SAPB block. The initial respiratory rate was 20 BPM with 19 mm of diaphragmatic excursion ( Image 4A ). After 60 minutes from the SAPB, the patient’s respiratory rate was 14 BPM with a diaphragmatic excursion of 32 mm (increase of 41%) ( Image 4B ).

(A) Pre-block demonstrating left-sided diaphragmatic excursion of 19 mm. (B) Post-block demonstrating left-sided diaphragmatic excursion of 32 mm (increase of 41%).

All blocks were performed by fellowship-trained ultrasound faculty. The vital signs of all the patients were stable; specifically, no patient had hypotension or hypoxia prior to the block being performed. No additional pain medications were given prior to the second diaphragmatic excursion exam.

To our knowledge this is the first description of using diaphragmatic excursion as a measurement of appropriate pain control in acute rib fractures. In our cases, after SAPB the respiratory rate decreased while M-mode measured diaphragmatic excursion increased. This initial data may suggest a new objective measure of improved pain control for acute rib fractures as well as decreased respiratory splinting. Ultrasound-measured diaphragmatic excursion may provide a much-needed objective measure of respiratory improvement in acute rib fracture, since subjective pain scores are typically the only measures used during clinical care. 12

Diaphragmatic excursion may also be used as a signal for overall pain. Pain can be evident in some patient populations by an increase in respiratory rate and more shallow breaths for all acute painful conditions. Diaphragmatic excursion may directly demonstrate improved pain control and respiratory function following ultrasound-guided peripheral nerve blocks, and not just for thoracic trauma as shown in these three cases. Although subjective pain scales have a role in measuring block effectiveness, they are an indirect measure of respiratory function and problematic in cases where there are distracting injuries or altered mental status. Diaphragmatic excursion, however, can be used in all patients and could define that ultrasound-guided nerve blocks both relieve pain in the form of decreased splinting as well as directly improve pulmonary function. This technique has the potential to be valuable both in future studies of nerve block effectiveness and to help guide adequate pain control in clinical situations where patients are not able to communicate subjective pain using visual pain scores.

The POCUS-measured diaphragmatic excursion is both easily learned and non-invasive, making it an ideal objective measure. Although this case series demonstrates diaphragmatic excursion as a promising novel tool to quantify pain and respiratory splinting, it has several limitations. Data regarding interrater reliability was not available as diaphragmatic measurements were obtained by a single clinician pre- and post-block. Although a standardized technique was used to measure diaphragmatic excursion, a possibility of measurement error exists from differences in probe placement pre- and post-block. Lastly, subjective pain scores pre- and post-block were only available for the third case, and spirometry data was not collected for comparison. Point-of-care ultrasound measured diaphragmatic excursion is both easily learned and non-invasive, making it an ideal objective measure.

Serratus anterior plane bock performed for acute rib fractures reduced pain in all three patients. It also increased the diaphragmatic excursion and decreased the respiratory rate in all three cases. Diaphragmatic excursion may be an alternative to visual pain scores to evaluate SAPB efficacy. More data will be needed to determine whether this same relationship can extend to other ultrasound-guided nerve blocks.

Section Editors: Christopher Sampson, MD

Full text available through open access at http://escholarship.org/uc/uciem_cpcem

The authors attest that their institution does not require Institutional Review Board approval. Patient has been obtained and filed for the publication of this case report. Documentation on file.

Conflicts of Interest : By the CPC-EM article submission agreement, all authors are required to disclose all affiliations, funding sources and financial or management relationships that could be perceived as potential sources of bias. The authors disclosed none.

Full text links 

Read article at publisher's site: https://doi.org/10.5811/cpcem.2022.7.57457

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• Introduction
• Palp/Percus
• Auscultation

Palpation/Percussion

Thoracic expansion:.

• Is used to evaluate the symmetry and extent of thoracic movement during inspiration.
• Is usually symmetrical and is at least 2.5 centimeters between full expiration and full inspiration.
• Can be symmetrically diminished in ankylosing spondylitis .
• Can be unilaterally diminished in chronic fibrotic lung disease , extensive lobar pneumonia, large pleural effusions, bronchial obstruction and other disease states.

Percussion:

Percussion is the act of tapping on a surface, thereby setting the underlying structures in motion, creating a sound and palpable vibration. Percussion is used to determine whether underlying structures are fluid-filled, gas-filled, or solid. Percussion:

• Penetrates 5 - 6 centimeters into the chest cavity.
• May be impeded by a very thick chest wall.
• Produces a low-pitched, resonant note of high amplitude over normal gas-filled lungs.
• Produces a dull, short note whenever fluid or solid tissue replaces air filled lung (for example lobar pneumonia or mass) or when there is fluid in the pleural space (for example serous fluid, blood or pus).
• Produces a hyperresonant note over hyperinflated lungs (e.g. COPD ).
• Produces a tympanitic note over no lung tissue (e.g. pneumothorax ).

Diaphragmatic excursion:

• Can be evaluated via percussion.
• Is 4-6 centimeters between full inspiration and full expiration.
• May be abnormal with hyperinflation , atelectasis , the presence of a pleural effusion , diaphragmatic paralysis, or at times with intra-abdominal pathology.

Assessment of diaphragmatic function by ultrasonography: Current approach and perspectives

Affiliations.

• 1 Institut de Recherche Biomédicale des Armées, ERRSO, Toulon 83800, France.
• 2 Service d'Explorations Fonctionnelles Respiratoires, CHU Nord, Assistance Publique des Hôpitaux de Marseille et Aix Marseille Université, IRD, APHM, MEPHI, IHU-Méditerranée Infection, Marseille 13015, France.
• PMID: 32607319
• PMCID: PMC7322428
• DOI: 10.12998/wjcc.v8.i12.2408

This article reports the various methods used to assess diaphragmatic function by ultrasonography. The excursions of the two hemidiaphragms can be measured using two-dimensional or M-mode ultrasonography, during respiratory maneuvers such as quiet breathing, voluntary sniffing and deep inspiration. On the zone of apposition to the rib cage for both hemidiaphragms, it is possible to measure the thickness on expiration and during deep breathing to assess the percentage of thickening during inspiration. These two approaches make it possible to assess the quality of the diaphragmatic function and the diagnosis of diaphragmatic paralysis or dysfunction. These methods are particularly useful in circumstances where there is a high risk of phrenic nerve injury or in diseases affecting the contractility or the motion of the diaphragm such as neuro-muscular diseases. Recent methods such as speckle tracking imaging and ultrasound shear wave elastography should provide more detailed information for better assessment of diaphragmatic function.

Keywords: Dysfunction; Hemidiaphragm; M-mode; Motion; Paralysis; Speckle tracking imaging; Thickness; Two-dimensional mode; Ultrasound; Ultrasound shear wave elastography.

©The Author(s) 2020. Published by Baishideng Publishing Group Inc. All rights reserved.

Publication types

• Open access
• Published: 16 November 2021

The role of diaphragmatic ultrasound as a predictor of successful extubation from mechanical ventilation in respiratory intensive care unit

• Randa Salah Eldin Mohamed 1 ,
• Abeer Salah Eldin Mohamed 1 ,
• Waleed Fouad Fathalah 2 ,
• Mohamed Farouk Mohamed 1 &
• Ahmed Aelgharib Ahmed 3  

The Egyptian Journal of Bronchology volume  15 , Article number:  51 ( 2021 ) Cite this article

2951 Accesses

2 Citations

Metrics details

A Correction to this article was published on 14 December 2021

This article has been updated

The diaphragm muscle whose dysfunction may be very common in patients undergoing mechanical ventilation (Ferrari G, De Filippi G, Elia F, Panero F, Volpicelli G, Aprà F. Crit Ultrasound J 6:8, 2014). Aim: To evaluate real-time ultrasound in the evaluation of diaphragmatic thickening, thickening fraction, and/or excursion to predict extubation outcomes. We aimed to compare these parameters with other traditional weaning measures is a fundamental.

Out of 80 included patients, 20 (25%) have failed extubation. Diaphragmatic thickening (DT), thickening fraction (DTF), and/or excursion (DE) were significantly higher in the successful group compared to those who failed extubation ( p < 0.05). Cutoff values of diaphragmatic measures associated with successful extubation (during tidal breathing) were ≥ 17 mm for DE; ≥ 2.1 cm for DT inspiration; ≥ 15.5 mm for DT expiration, functional residual capacity (FRC); and ≥ 32.82% for DTF %, giving 68%, 95%, 62%, and 90% sensitivity, respectively, and 65%, 100%, 100%, and 75% specificity, respectively. Cutoff values of diaphragmatic parameters associated with successful extubation (during deep breathing) were > 28.5 mm DT Insp, total lung capacity (TLC); >22.5mm DT Exp (RV); >37 DTF %; and > 31 mm DE, giving 100%, 73%, 97%, and 75% sensitivity and 65%, 75%, 100%, and 55% specificity, respectively. Rapid shallow breathing index (RSBI) had 47% sensitivity but 90% specificity.

Ultrasound evaluation of diaphragmatic parameters could be a good predictor of weaning in patients who passed the T-tube.

The diaphragm is an important respiratory muscle, and dysfunction is very common in patients receiving mechanical ventilation. Diaphragm fatigue occurs even in patients who successfully pass the spontaneous breathing test (SBT) [ 1 ]. Interrupting ventilation too early can lead to increased cardiovascular and respiratory pressure (CO2) retention and hypoxemia with up to 25% of patients requiring reinstitution of ventilator support. Unnecessary delays in liberation from mechanical ventilation also can be deleterious. Complications such as ventilator-associated pneumonia and ventilator-induced diaphragm atrophy can be seen with short periods of mechanical ventilation, thereby prolonging mechanical ventilation [ 2 ]. As SBT monitoring is insensitive to detect early signs of load-capacity imbalance [ 3 ], the evaluation of the diaphragmatic thickening fraction (DTF) may be also helpful to assess diaphragmatic function and its contribution to respiratory workload [ 1 ]. Ultrasound can be used to detect the deflection of the diaphragm, which helps to identify patients with diaphragm dysfunction [ 4 ].

This prospective study was carried out on 40 patients who are mechanically ventilated due to pulmonary disease, 40 patients on mechanical ventilation due to non-pulmonary disease at respiratory ICU, and 40 chronic obstructive pulmonary disease (COPD) patients from an outpatient clinic serving as controls at Embaba Chest Hospital, Cairo, Egypt, during a period from January 2018 to November 2019. Written informed consent was obtained from all patients prior to enrollment according to approval at the local committee of Beni-suef University Hospital. Patients on mechanical ventilation due to pulmonary disease (pneumonia, COPD, bronchial asthma, bronchiectasis …. etc.) and non-pulmonary disease (pulmonary edema, myocardial infarction, etc.) were included in this study. Patients with pneumothorax, pleural effusion, neuromuscular diseases, and suspicious diaphragmatic paralysis (raised copula in chest X-ray); patients with pleurodesis; and patients who presented with stridor (due to upper airway involvement due to mechanical ventilation in last 6 months) were excluded from this study.

Study design

Patients were assessed by the following: Acute Physiology and Chronic Health Evaluation II (APACHE II) score, Charlson comorbidity index (CCI), and diaphragm ultrasound. M-mode ultrasound was used to assess diaphragmatic excursion, and movement B-mode ultrasound was used to assess diaphragmatic thickness. Once patients were stable and both ventilator and biochemical parameters were accepted for weaning, T-tube was attempted for 2 h. Patients who passed the SBT on T-tube were included in data analysis and followed up for 48h after extubation where they received oxygen through Venturi mask or nasal oxygen and followed up for 48 h after extubation. Successful extubation was defined as maintenance of spontaneous breathing for > 48 h following extubation. Extubation failure was defined as the inability to maintain spontaneous breathing for at least 48 h, without any ventilatory support. All patients were studied with the head of the bed elevated between 20 and 40°. Diaphragmatic thickness (DT) was measured using a 7–10-MHz linear ultrasound probe set to B-mode. The right hemidiaphragm was imaged at the zone of apposition of the diaphragm and rib cage in the midaxillary line between the 8th and 10th intercostal spaces. The DT was measured at end expiration and end inspiration. The percent change in DT between end expiration and end inspiration (DTF %) was calculated as (DT end inspiration − DT end expiration/DT end expiration) × 100 [ 5 ].

Diaphragmatic excursion (DE)

The convex probe is placed in the right subcostal region parallel to the intercostal space to measure the range of the diaphragmatic movement using the M-mode method with the cursor crossing the diaphragm to assess the highest and lowest points as an indicator for the diaphragmatic mobility range [ 6 , 7 ]. The maneuver was repeated at least three times and the average measurement is taken. Measurement of diaphragmatic thickness and excursion was recorded during tidal breathing and deep breathing (Fig. 1 ).

M-mode of diaphragm excursion ( A ) and B-mode of diaphragm thickness ( B , inspiration; C , expiration)

Criteria of weaning

The criteria of weaning are 1- positive end-expiratory pressure (PEEP) ≤ 5 cm H2O 2- Fraction of inspired oxygen (FiO2) < 0.5 3- Respiratory rate (RR) < 30 breaths/min 4- rapid shallow breathing index < 105, and PaO2/FiO2 > 200.

Criteria for failure

The criteria for failure are change in mental status, onset of discomfort, diaphoresis, respiratory rate > 35 breaths/min, and hemodynamic instability (heart rate > 140, systolic blood pressure >180) [ 8 ]. Patients were divided into two groups: group A included 40 patients on mechanical ventilation due to pulmonary diseases to compare parameters of weaning to diaphragmatic thickness and excursion during tidal breathing and deep breathing. Group B includes 40 patients on mechanical ventilation due to non-pulmonary diseases to compare parameters of weaning to diaphragmatic thickness and excursion during tidal breathing and deep breathing.

The collected data was revised, coded, tabulated, and introduced to a PC using the Statistical Package for Social Science (SPSS 17). Data was presented and suitable analysis was done according to the type of data obtained for each parameter. The distributions of quantitative variables were tested for normality. Quantitative data were described using mean and standard deviation for normally distributed data while abnormally distributed data was expressed using the median. For normally distributed data, comparisons between both groups were done using an independent t -test, while abnormally distributed data was assessed using the Mann-Whitney test. A receiver operator characteristic curve (ROC curve) was used to find out the best cutoff value and the validity of a certain variable. Agreement of the different predictive values of the outcome was used and was expressed in sensitivity, specificity, positive predictive value, and negative predictive value.

During the study period (Fig. 2 ), we evaluated 162 patients ready for weaning. Forty chronic obstructive pulmonary disease (COPD) patients (stable) served as a control group. Forty-two patients were excluded, 10 of which had pleural effusion, 4 patients had pneumothorax, 10 patients had diaphragmatic paralysis, and 18 patients were non-cooperative. Eighty patients (on T-tube) undergoing SBT were divided into two groups: group A included 40 patients (non-pulmonary-related cause) and had their diagnosis as follows: 24 (60%) had congestive heart failure, 4 (10%) had diabetes mellitus, 4 (10%) had sepsis other than pneumonia, 2 (5%) had epilepsy, 2 (5%) had embolic hemiplegia, and 4 (10%) had chronic renal failure. Out of group A patients, 9 patients (11.25%) had failed weaning of which 4 patients needed reintubation and 5 patients needed non-invasive positive ventilation of which 2 patients were reintubated and 3 patients died. Group B included 40 patients (pulmonary-related cause) and had their diagnosis as follows: 21 (53%) had COPD, 8 (20%) had asthma, 5 (13%) had bronchiectasis, 5 (13%) had pneumonia, and 1 (3%) had viral influenza H1N1. Out of group B patients, 11 patients (13.75%) had failed weaning, of which 6 patients needed reintubation and 5 patients needed non-invasive positive ventilation of which 3 patients were reintubated and 2 patients died. Regarding ultrasound diaphragmatic parameters (during tidal breathing) (Table 1 ), DT Insp mm, DT Expt (FRC) mm, DTF %, and DE in centimeters were significantly higher [24 mm (23.25–26) vs.18 mm (17–19.15), p < 0.001; 17 mm (15–18) vs.14 mm (12.3–15), p < 0.001; 44.41% (35.07–67.12) vs. 30.38% (23.34–38.07), p < 0.001; 1.95 cm (1.53–2.75) vs. 1.66 cm (1.09–1.94), p <0.003]. Regarding ultrasound diaphragmatic parameters during deep breathing (Table 1 ), DT Insp (TLC) mm, DT Exp (RV) mm, DTF %, and DE in cm were significantly higher [36.5 mm (33–39.75) vs. 26 mm (23.25–29.75), p < 0.001; 25 mm (22–27) vs. 20.5 mm (18–22.75), p < 0.001; 50% (43.05–58.2) vs. 25% (23.8–26.99), p < 0.001; 3.6 cm (3–5.4) vs. 2.95 cm (1.73–4.05), p < 0. 0.01] respectively in the successfully extubated group compared to the failed one (Table 1 ). AUC was used to assess the accuracy of diaphragmatic parameters in predicting failed extubation (during tidal breathing) (Table 2 ) (Fig. 3 ). A cutoff value of DT Exp (FRC) > 15.5mm was associated with successful extubation with 62% sensitivity and 100% specificity, a cutoff value of DTF % > 32.82 was associated with successful extubation with 90% sensitivity and 75% specificity, a cutoff value of DE > 1.7 cm was associated with successful extubation with 68% sensitivity and 65% specificity, and the optimum cutoff value of DT Insp > 21 mm was associated with successful extubation with 95% sensitivity and 100% specificity (Table 2 ) (Fig. 3 ). A cutoff value (during deep breathing) of DT Exp (RV) > 22.5 was associated with successful extubation with 73% sensitivity and 75% specificity, a cutoff value of DE > 3.1 was associated with successful extubation with 75% sensitivity and 55% specificity, a cutoff value of DT Insp (TLC) > 28.5mm was associated with successful extubation with 100% sensitivity and 65% specificity, and the optimum cutoff value of > 37 DTF % was associated with successful extubation with 97% sensitivity and 100% specificity but AUC 100% (Table 2 ) (Fig. 4 ). Among the traditional weaning parameter (RSBI, minute ventilation, RR, and PaO2/FiO2), PaO2/FiO2 was significantly more in the successful extubation group than the failed one [206 (197.3–211.8) vs. 190 (185–199.8), p < 0.0.001] (Table 1 ) (Fig. 5 ). All DT parameters were significantly higher in the COPD group than in failed weaning in the pulmonary group (B) (Table 3 ).

Flow chart showing criteria of patients’ selection and follow-up through the study

ROC curve of diaphragmatic parameters during tidal breathing

ROC curve of diaphragmatic parameters during deep breathing

ROC curve of RR, MV, and RSBI in the prediction of successful weaning

The diaphragm is the main respiratory muscle, which plays an important role in the respiratory movement, and its dysfunction predisposes to prolonged duration of mechanical ventilation and respiratory complications. Sonographic evaluation has recently started to become popular in the intensive care unit (ICU) for assessing diaphragmatic function [ 9 ]. In comparing the control COPD cases with others who suffered from MV with failed weaning experience, regarding US parameters during tidal breathing, both of inspiratory, expiratory DT, DE, and DTF % were significantly higher in the COPD group (control) than in the failed weaning group (B) ( p < 0.001). Furthermore, during deep breathing techniques, all DT parameters were significantly higher in the COPD group than in the weaning failure group ( p < 0.001). In our knowledge, this is the first study that compared pulmonary diseases and COPD as regards the diaphragmatic ultrasound parameter (Table 3 ).

Diaphragmatic thickness during tidal breathing (Fig. 3 )

In the present study, DT at end inspiration in the successful group was 24 mm (23.25–26), versus failed group 18 mm (17–19.15), p < 0.001, with a cutoff point > 21mm, 95% sensitivity, 100% specificity, 100% PPV, 99% NPV, and an AUC 95% (Tables 1 and 2 ). Similarly, Farghaly and Hasan [ 3 ] found DT at end inspiration in a successful group was 24 mm (22–28), versus failed group 18 mm (15–20), with a cutoff point ≥ 21 mm, 77.5% sensitivity, 86.6% specificity, and an AUC of 83.1%. In the present study, DT (FRC) at end expiration in a successful group was 17 mm (15–18), versus failed group 14 mm (12.3–15), p = 0.001, with a cutoff point >15.5%, 62% sensitivity, 100% specificity, 100% PPV, 92% NPV, and an AUC 85% (Tables 1 and 2 ) (Fig. 3 ). Similarly, Farghaly and Hasan found that DT at end expiration in a successful group was 16 mm (11.2–18.7), versus failed group 11 mm (10–15), with a cutoff point ≥ 10.5 mm, 80% sensitivity, 50% specificity, and an AUC 68.8% [ 3 ]. In the present study, DTF% in a successful group was 44.41% (35.07–67.12), versus failed group 30.38% (23.34–38.07), with a cutoff point > 32.82%, 90% sensitivity, 75% specificity, 44% PPV, 97% NPV, and an AUC 77% (Tables 1 and 2 ) (Fig. 3 ). This result is consistent with studies by Farghally and Hasan [ 3 ] and Dinino et al. [ 10 ] which demonstrated that DTFs with a cutoff point more than 34 and 30, respectively, were associated with weaning success and better ICU outcomes. In contrast with Umbrello et al. [ 4 ], who observed patients after major elective surgery and first weaning failure, they reported that a cutoff point of DTF more than 20% was associated with weaning success, and this may be explained by the absence of surgical patients in this study. In the present study, DE in a successful group is 1.9 cm (1.53–2.75), versus failed group 1.66 cm (1.09–1.94), p = 0.001, with a cutoff point > 1.7 cm, 68% sensitivity, 65% specificity, 30% PPV, 90% NPV, and an AUC 0.73 (Tables 1 and 2 ) (Fig. 3 ). This result is consistent with the studies done by Matamis et al. [ 9 ] and Palkar et al. [ 11 ] who confirmed that DE at a cutoff point of more than 1.65 cm and 1.64 cm, respectively, was associated with weaning success and better ICU outcomes. Also, Gursel et al. [ 12 ] reported that tidal diaphragmatic excursion using standard ultrasound devices (SD) is 1.76 ± 0.69 cm (0.58–3.30) and using pocket-sized ultrasound devices (PSDs) 1.62 ± 0.70 cm (0.50–3.00). In the present study, the AUC of the DT Insp (95) was more than that of DTF (77), while AUC of DT Exp (FRC) (85) was more than that of DTF (77). In contrast, Farghaly and Hasan stated that AUC of DT (83.1) at end inspiration was more than DT (68.8) at the end expiration and AUC of DT (68.8) at the end expiration was less than DTF (70. 8). Also, it was found that AUC of DT (61) at the end expiration was less than that of DTF (79) alone [ 3 ]. In the present study, the DE was less (68%) sensitive than that DT Insp (95%), and the specificity of DT Insp (100%) was more than that of DE (30%) (Table 2 ). Similarly, Farghaly and Hasan observed that diaphragm excursion should not be used in the assessment of diaphragmatic contractile activity, whereas diaphragm thickening is a good indicator of respiratory effort [ 3 ]. Also, Umbrello et al. observed that during pressure support ventilation, diaphragm thickening was more accurate than diaphragm excursion and suggested that the use of diaphragm excursion is of little help during PSV and should not be used in the assessment of diaphragmatic contractile activity [ 4 ]. In contrast, Hayat et al. [ 13 ] reported that diaphragmatic excursion is a good method for predicting the weaning outcome.

Diaphragmatic thickness during deep breathing

In the current study, diaphragm thickness at TLC in a successful group was 36 mm (33–39.75), versus failed group 26 mm (23.25–29.75) with a cutoff point 28.5, 100% sensitivity, 65% specificity, 39% PPV, 100% NPV, and an AUC 0.87, while diaphragm thickness at RV in the successful group was 25 mm (22–27), versus failed group 20.5 mm (18–22.75) with a cutoff point 22.5 mm, 73% sensitivity, 75% specificity, 39% PPV, 93% NPV, and an AUC 0.75 (Tables 1 and 2 ) (Fig. 4 ). Similarly, Ferrari et al. stated that diaphragm thickness (DT) at TLC in a successful group was 38 mm (29–45), versus failed group 30 mm (20–40) [ 1 ], while DT at RV in a succeeded group was 25 mm (19–28), versus failed group 24 mm (17–30). Moreover, Gursel et al. found that the maximal inspiratory thickness was SD 47 ± 16mm (23–68) and PSDs 45 ± 12mm (24–91). In contrast, Pirompanich and Romsaiyut noted that DT at TLC in a succeeded group was 35 ± 13 and 38 mm (IQR 29–45), versus failed group 31 ± 13 mm and 30 mm (IQR 20–40) [ 12 ], while diaphragm thickness at RV in a successful group was 22 ± 09 mm and 25 mm (IQR 19–28), versus failed group 25 ± 11 mm and 24 mm (IQR 17–30).There were higher values about RV in the failed group more than the successful group, and these variables can be explained by different causes for mechanical ventilation as well as different ventilation periods and different ethnic groups which may affect the thickness of the diaphragm. In the present study, DTF in a successful group was 50% (43.05–58.20), versus failed group 25% (23.80–26.99), with a cutoff point of 37%, 97% sensitivity, 100% specificity, 97% PPV, 100% NPV, and an AUC 1 (Tables 1 and 2 ) (Fig. 4 ). These results are consistent with studies done by Ferrari et al. [ 1 ] which demonstrated that DTFs of more than 36% were associated with weaning success and better ICU outcomes. Our study found that DE in a successful group was 3.6 cm (3–5.4), versus failed group 2.95 cm (1.73–4.05), with a cutoff point DE 3.1 cm, 75% sensitivity, 55% specificity, 27% PPV, 91% NPV, and an AUC 0.68 (Tables 1 and 2 ) (Fig. 4 ). Similarly, Carrie et al. found that DE in the successful group was 4.1 ±2. 1cm, versus failed group 3 ± 1.8cm with a cutoff point DE 2.7cm [ 14 ]. Also, Gursel et al. found in their study DE (±SD) was 2.97 ± 1.18cm (1.33–5.40) and PSDs 2.67 ± 0.90cm (1.30–4.70) [ 12 ]. Moreover, Lerolle et al. reported that DE less than 2.5 cm was a predictor of weaning failure, in post-cardiac patients connected to mechanical ventilation [ 15 ]. In the present study, the DTF was more specific and sensitive with a higher AUC (100%, 97%, 1) than DE (55%, 75%, 0.91) (Table 2 ) (Fig. 4 ). This result is consistent with the studies by Samanta et al. [ 16 ] and Ferrari et al. [ 1 ] who reported that the DTF is more accurate than DE in the prediction of successful weaning. In the present study, DT Insp (TLC) is more sensitive and specific (100%, 65%) than DE (75%, 55%). The AUC of DT Insp (TLC) was more than that of DT Exp (RV) (0.87 and 0.75, respectively). The AUC of DTF was more than the AUC of DT Insp (TLC) (100 and 87, respectively) (Table 2 ) (Fig. 4 ). In contrast, Farghaly and Hasan observed that the AUC of DT at end inspiration was more than DT at end expiration (83.1 and 68. 8, respectively) [ 3 ]. Also, Di Nino et al. observed that the AUC for DT end expiration was less than that for DTF% alone (0.79 and 0.61, respectively) [ 10 ]. However, they determined DT, DTF, and DE during tidal breathing, while in the current study, DT, DTF, and DE were assessed during tidal and deep breathing. In the present study, the AUC of DTF during deep breathing was more than DT Insp during tidal breathing (100 and 95, respectively), while the AUC of DT Insp was more than DT Insp (TLC) (95 and 87, respectively) (Table 2 ). In the present study, the RSBI in the successful group was 58 (52–63) breath/min/L, versus failed group 46 (41–51) breath/min/L, p < 0.005, and a cutoff value for RSBI was 35.5 b/min with 47% sensitivity, 90% specificity, 51% PPV, 188% NPV, and the AUC of 71% in predicting extubation failure (Tables 1 and 2 ) (Fig. 5 ). Similarly, Farghaly and Hasan observed that the RSBI in a successful group was 51.5 (44–79), versus failed group 50 (40–65), p <0.005 [ 3 ]. Also, Pirompanich and Romsaiyut found that the average RSBI in a successful group was 54. 3 ± 22.8, versus failed group 47.7 ± 14.8, p < 0.012 [ 14 ]. In contrast, Ferrari et al. observed that the RSBI in a successful group was 70 (57–83), versus failed group 120 (110–148), p < 0.0001 [ 1 ]. This variation can be explained by different causes for mechanical ventilation as well as different ventilation periods, which may affect the outcome of the weaning process. During tidal breathing, the specificity of RSBI was less than DT at insp and DT Exp (FRC) at end expiration (90, 100, and 100). But the specificity of RSBI is more than DTF and DE (90, 75, and 65). But the AUC of RSBI is less than DT Insp, DT Exp (FRC), DTF, DE, TLC, RV, and DTF (71, 95, 85, 77, 73, 87, 75, and 100, respectively). The AUC of RSBI during forced expiration and inspiration is more than DE (71 and 68, respectively) (Table 2 ) (Figs. 3 , 4 , and 5 ). Similarly, DiNino et al. reported that the diaphragmatic thickness and diaphragmatic thickness fraction are more accurate than RSBI, for predicting successful weaning [ 10 ]. Also, Pirompanich and Romsaiyut observed that integration of DTF (right) (AUC 95%) and RSBI (AUC 70%) are more accurate than RSBI (AUC 70%), for foretelling of successful extubation [ 17 ]. Similarly, Farghaly and Hasan reported that the diaphragm thickness, DTF, and DE during tidal breathing are more accurate than RSBI [ 3 ]. They recommended to consider the use of these parameters with RSBI to improve weaning outcome. In addition, Hayat et al. reported that the DE during tidal breathing is more accurate than RSBI, but they did not use DT and DTF in the comparison [ 13 ]. Ramakrishnan and Siddiqui reported that the diaphragmatic excursion is probably better in predicting extubation success than RSBI [ 18 ].

Fate of the studied patients

In the present study, as regards group A, the number of patients with successful weaning was 31 (77.5%) versus 9 (22.5%) of weaning failure, while in group B, the number of patients with successful weaning was 29 (72.5%) versus 11 (27.5%) of weaning failure. This is consistent with Esteban et al. [ 8 ], 27%. This is in contrast with Ferrari et al. [ 1 ] who reported a 63% failure rate. This variation can be explained by different causes for mechanical ventilation as well as different ventilation periods before starting the weaning process, which may affect the outcome of the weaning process.

Study limitations

The measurements of the diaphragm were not supplemented with direct measurements (such as the maximal expiratory pressure, maximal inspiratory pressure, and transdiaphragmatic pressure). This study was done in the respiratory care unit, and there were no surgical treated patients. While the (reference) thickness of the diaphragm in many diseases, e.g., COPD, pneumonia, and DM, is still unknown, the golden standard of measuring the diaphragmatic strength is phrenic nerve stimulation, and comparing it with sonographic findings was not done in this study. This study did not target a certain chest disease in its assessment of the diaphragm. The right hemidiaphragm was used in the diaphragmatic assessment being easier in imaging than the left hemidiaphragm which is often impeded by intestinal and gastric gas.

Conclusions

Ultrasound of the diaphragm is a simple, easy, non-invasive, and inexpensive method useful to evaluate the thickness of the diaphragm in the zone of apposition. Assessment of DT, DTF by diaphragm ultrasound in B-mode, and DE in M-mode represents a new weaning index with highly accurate results in comparison to the other traditional indices as RSBI, so they can be used as predictive parameters to assess the weaning process outcome.

Ultrasound of the diaphragm is a simple, easy, non-invasive, and inexpensive method useful to evaluate the diaphragmatic muscle. Parameters like diaphragmatic thickness and diaphragmatic excursion can be recorded by real-time ultrasound and could have many clinical reflections. The diaphragmatic thickness fraction during deep breathing could be a good foreteller of weaning from mechanical ventilation.

What this paper contributes to our knowledge

Assessment of diaphragmatic thickness, by diaphragmatic ultrasound in B-mode and diaphragmatic excursion in M-mode, can be used as predictive parameters to assess the weaning process outcome in patients on mechanical ventilation.

Availability of data and materials

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Change history

14 december 2021.

A Correction to this paper has been published: https://doi.org/10.1186/s43168-021-00103-9

Abbreviations

Acute Physiology and Chronic Health Evaluation II

Brightness mode

Charlson comorbidity index

Chronic obstructive lung disease

Control mechanical ventilation

Computerized tomography

Diaphragmatic excursion

Diabetes mellitus

Diaphragmatic thickness

Diaphragmatic thickness at the end expiration

Diaphragmatic thickness fraction

Diaphragmatic thickness at end inspiration

• Diaphragmatic ultrasound

Functional residual capacity

Focus thoracic ultrasound

Hypertension

Intensive care unit

Ischemic heart disease

Interquartile range

Inferior vena cava

Lung ultrasound

Motion mode

Magnetic resonance imaging

Mechanical ventilation

Non-invasive ventilation

Negative predictive value

Prolonged mechanical ventilation

Positive predictive value

Pocket-sized ultrasound devices

Pressure support ventilation

Transdiaphragmatic pressure

Rapid shallow breathing index

Residual volume

Spontaneous breathing

Standard ultrasound devices

Standard deviation

Spatial pulse length

Diaphragm thickness at functional residual capacity

Total lung capacity

Thoracic ultrasound

Ventilator-induced diaphragmatic dysfunction

Tidal volume

Two-dimensional

Three-dimensional

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Acknowledgements

We would like to express our great gratitude to the National Institute Chest Hospital for their great support.

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Department of Pulmonology, Beni Suef University Faculty of Medicine, Beni Suef, Egypt

Randa Salah Eldin Mohamed, Abeer Salah Eldin Mohamed & Mohamed Farouk Mohamed

Department of Endemic Medicine and Hepatology, Cairo University Kasr Alainy Faculty of Medicine, Cairo, Egypt

Waleed Fouad Fathalah

National Institute of Chest Hospital, 2 street Talat harb, Giza, Egypt

Ahmed Aelgharib Ahmed

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AA collected the patient’s data and wrote the initial manuscript, WF did the ultrasonic assessment of the diaphragm and revised the manuscript, MF performed workup and sample analysis, ASM performed the computations and verified the analytical methods, and RSM revised the manuscript. MF, ASM, and RSM were major contributors in writing the manuscript, supervised, and reviewed the data collection and statistical analysis. All authors read and approved the final manuscript.

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Correspondence to Ahmed Aelgharib Ahmed .

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Mohamed, R.S.E., Mohamed, A.S.E., Fathalah, W.F. et al. The role of diaphragmatic ultrasound as a predictor of successful extubation from mechanical ventilation in respiratory intensive care unit. Egypt J Bronchol 15 , 51 (2021). https://doi.org/10.1186/s43168-021-00095-6

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Role of diaphragmatic ultrasound in predicting weaning success from mechanical ventilation in pediatric intensive care unit

• Amir Maurice Eskander   ORCID: orcid.org/0009-0001-4657-3360 1 ,
• Abeer Maghawry Abd-Elhameed 1 ,
• Noha Mohamed Osman 1 ,
• Sondos Mohamed Magdy 2 &
• George Ezzat ElKess 1  

Egyptian Journal of Radiology and Nuclear Medicine volume  55 , Article number:  114 ( 2024 ) Cite this article

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Metrics details

Weaning off mechanical ventilation (MV) is a critical step in pediatric ICU; however, it lacks standardized criteria. Diaphragmatic ultrasound parameters like diaphragm thickening fraction (DTF), diaphragmatic excursion (DE) and time to peak inspiratory amplitude (TPIA) can be used to assess diaphragmatic muscle strength and to predict weaning success.

Aim of study

Is to assess the validity of diaphragmatic ultrasonography as a predictor of weaning outcome from mechanical ventilation in pediatric age group.

Prospective cohort study including 30 pediatric patients aged 0–18 years on mechanical ventilation. Ultrasound measurements of diaphragmatic thickening fraction, diaphragmatic excursion and time to peak inspiratory amplitude were taken during the spontaneous breathing trial (SBT) and compared between successful and failed weaning groups.

Out of the included 30 patients (50% male), 19 patients (63.3%) were successfully weaned. Mechanical ventilation duration was significantly longer in the failed weaning group ( P  = 0.017). There was significant difference between both groups regarding right DE ( P  = 0.032) and left DE ( P  = 0.022) with cutoff values of > 4.1 mm and > 5.5 mm with AUC (Area under curve) of 0.737 and 0.831, respectively. There was no statistically significant difference between both groups regarding DTF or TPIA.

We have found that DE is a predictor of weaning success, while DTF and diaphragmatic TPIA had no correlation with weaning outcome.

Mechanical ventilation (MV) is widely used in pediatric intensive care units (PICU). About one-third of PICU patients need MV support. However, MV support is not the end of the treatment, and the goal is to help patients wean off MV support. Weaning is a crucial transition for every patient and its optimal timing can decrease the duration of MV and reduce complications [ 1 ].

In pediatric population, there is no defined standard for weaning, and no ideal ventilator settings that is agreed upon to wean children in PICU [ 2 ]. Currently, weaning from MV is mainly a clinical judgment subjective decision, leading to extreme variations in weaning decisions and inevitable weaning failure [ 3 ].

Multiple factors must be present for successful weaning, including hemodynamic stability and adequate ventilation/perfusion ratio of the patient in addition to ability to generate a strong cough, expectorate endotracheal secretions and generate a reliable ventilator pattern. All these factors are affected by decreasing lung aeration, alterations in pulmonary compliance and diaphragmatic dysfunction resulting from prolonged MV [ 4 ].

It has been established in adults that prolonged MV leads to ventilator-induced diaphragmatic dysfunction (VIDD) which is basically atrophy and dysfunction of the diaphragm, leading to MV-induced loss of diaphragmatic force-generating capacity contributing to a longer weaning time and higher mortality [ 2 , 5 ].

Ultrasound being portable, fast and safe as well providing real-time morphologic and functional information, can play an important role in assessing two crucial factors among those that influence weaning: the aeration of the pulmonary parenchyma and the diaphragmatic function, providing clues on the probability of weaning success [ 4 ].

In adults, multiple studies have demonstrated the ability of diaphragmatic ultrasound to predict weaning success, leading to better decisions in weaning patients from MV. Conversely, in pediatric population, there are few studies exploring the role of diaphragmatic ultrasound in weaning in PICU, leading to insufficient conclusions. Moreover, children and adults vary widely in their respiratory physiology and anatomical characteristics [ 1 ].

Diaphragmatic ultrasound assesses the diaphragmatic function and contractility by measuring the diaphragm thickening during inspiration which is called diaphragmatic thickening fraction (DTF) and correlates strongly with diaphragmatic strength [ 5 ]. Another parameter measured is the diaphragmatic excursion (DE), which represents the vertical distance moved by the diaphragm during the respiratory cycle and reflects the respiratory effort exerted by the patient [ 4 ].

Time to peak inspiratory amplitude (TPIA) is a newly proposed diaphragmatic ultrasound parameter which is the time from the beginning of diaphragmatic contraction to the maximal amplitude of diaphragmatic inspiratory excursion. It was shown that longer TPIA correlated with more successful weaning from MV, suggesting that TPIA could be a marker for diaphragmatic strength [ 6 ].

The aim of this study is to assess the validity of diaphragmatic ultrasonography as a predictor of weaning outcome from mechanical ventilation in pediatric age group.

After ethical committee approval, a prospective cohort study was carried at our pediatric intensive care unit (PICU) of the children Hospital of Ain Shams University, Cairo, Egypt, starting from July 2021 to June 2023.

Study population

We included patients < 18 years in our PICU with acute respiratory failure connected to invasive mechanical ventilation for more than 24 h and eligible for weaning according to the following criteria: Reversal of the principal cause of mechanical ventilation, PaO 2  ≥ 60 mmHg, FiO 2  ≤ 0.40, PEEP ≤ 5 cmH 2 O, ratio of PaO 2 to FiO 2  ≥ 200, PH ≥ 7.30; RR ≤ 45/m, HR ≤ 140/min, RSBI ≤ 8 breaths/min/ml/kg body weight, minimal use of inotropic or vasopressor drugs, stable body hemodynamics, adequate consciousness level, does not receive sedatives or neuromuscular blocking drugs, absence of hemorrhage or anemia and no electrolyte disturbance. We excluded patients having; chronic neuromuscular disorder, known congenital heart, lung, or pleural malformation, unilateral/bilateral absence of diaphragmatic mobility in ultrasound, cervical spinal cord injury, pneumothorax, pleural effusion, ascites and those undergone thoracic or esophageal surgeries needing diaphragmatic manipulation.

Sample size calculation

Based on data present in the literature in 2020 mainly the work of Xue et al. [ 1 ] and Abdel Rahman et al. [ 7 ] and expected rate of successful weaning = 60%, our study included a convenience sample of 30 patients.

Study procedures

Informed consent from the patients’ guardians was acquired. Detailed history and anthropometric measurements were recorded. Once the patient is eligible for weaning, a spontaneous breathing trial (SBT) was commenced using low level of pressure support (5 cm H 2 O). Diaphragm and lung ultrasound were performed during the SBT. Treating clinicians were blinded to the results of the lung ultrasound score and diaphragm measurements. If the patient is eligible for extubation, he was followed up for 48 h to record the need for assisted ventilation (Invasive or noninvasive) post-extubation, and accordingly, patients were divided into two groups:

Successful weaning group: Defined as successful extubation and no need for noninvasive ventilation (NIV) or reintubation within 48 h.

Failed weaning group: Failed SBT or when there is need for reintubation or NIV within 48 h.

• Diaphragmatic ultrasound

All US measurements were performed using Samsung HM70A Ultrasound machine using the LA3-16AD 3–16 MHz Linear Array Transducer and the CF4-9 4–9 MHz Microconvex Array Transducer with all the US examinations done by a single trained radiologist to avoid any inter-observer variation. Patients were imaged in a semi-recumbent position with the head of bed at a 30-degree angle. Measurements were made of the right and left hemidiaphragms and repeated in three different respiratory cycles and an average was taken. For each side, three measurements were taken: DTF, DE and TPIA.

DTF was calculated by the following equation: DTF = (Thickness at the end inspiration – thickness at the end expiration)/Thickness at the end expiration × 100. It was measured in B-mode by placing the linear ultrasound probe in the 8th or 9th intercostal space between the anterior and midaxillary line in a perpendicular position to the chest wall an area designated the zone of apposition. Thickness of the diaphragmatic muscle was measured from the central point of the pleural line to the central point of the peritoneal line during the termination of inspiration and the termination of expiration (Fig.  1 ).

Measuring diaphragmatic thickness to calculate DTF using linear array probe. A Measuring at end inspiration with lung visible in the image due to caudal displacement of the diaphragm. B Measuring at end expiration

DE and TPIA were measured in M-mode by placing the microconvex 4–9 MHz ultrasound probe either a subcostally or intercostally in the mid-clavicular line, or in the right or left anterior axillary line. The liver or spleen was used as an acoustic window for each hemidiaphragm which appears as an echogenic line. The ultrasound probe was placed in the direction in which the ultrasound beam reaches the posterior third of the corresponding hemidiaphragm perpendicularly usually cranially, medially and dorsal. During inspiration, the normal diaphragm moves caudally toward the ultrasound transducer, which is recorded as an upward motion of the M-mode tracing and the reverse occurs during expiration.

DE is the vertical distance in millimeters between the highest and lowest peak points in the M-mode tracing while TPIA is the time from the beginning of diaphragmatic contraction to the maximal amplitude of diaphragmatic inspiratory excursion (Fig.  2 ).

Measuring right DE and diaphragmatic TPIA using microconvex probe in M-Mode. Liver is providing excellent acoustic window

Study outcome

Compare diaphragmatic ultrasound measurements (DTF, DE and TPIA) between successful and failure weaning groups to assess their value in prediction of weaning outcome.

Statistical methods

The quantitative data were presented as mean, standard deviations and ranges when parametric and median, inter-quartile range (IQR) when data found nonparametric. Qualitative variables were presented as number and percentages. The comparison between groups with qualitative data was done by using Chi-square test. The comparison between two independent groups with quantitative data and parametric distribution was done by using independent t test while with nonparametric distribution was done using Mann–Whitney test.

The study was conducted on 30 PICU patients. Nineteen patients (63.3%) were successfully weaned. Demographic, clinical and US data of our study is summarized in Table  1 . We found no significant association between both groups in regard to their age, gender or BMI.

Clinically there was a statistically significant correlation between duration of ventilation and weaning outcome ( P  = 0.017) where successful weaning group had shorter duration of MV.

Regarding diaphragmatic US measurements, we were only able to visualize the left diaphragm using the microconvex probe to measure DE and TPIA in 17 patients (56.7%). We found statistically significant correlation between the right and left DE and the weaning outcome ( P  = 0.032 and 0.022, respectively). We found no statistically significant correlation between right and left DTF or TPIA and weaning outcome.

ROC analysis of the right and left DE performance for the prediction of weaning failure or success was done (Table  2 ). The best cutoff value of excursion on the right side for predicting weaning success was ≥ 4.1 with an AUC of 0.737, the application of this threshold resulted in a sensitivity of 84.2% and a specificity of 54.55%. The best cutoff value of excursion on the left side for predicting weaning success was ≥ 5.5 with an AUC of 0.831, the application of this threshold resulted in a sensitivity of 54.5% and a specificity of 100%.

The feasibility of using diaphragmatic ultrasound indices in predicting the weaning success from MV in adults has been demonstrated in multiple studies [ 8 , 9 ] and although US is extensively employed in PICUs for echocardiographic and lung assessments, its application for diaphragm studies within pediatric intensive care settings is relatively recent. At the start of this study, there was limited studies regarding this topic in the pediatric age group [ 1 , 2 , 7 ] with more yet conflicting data emerging during the study period [ 10 , 11 , 12 , 13 , 14 ]. In our study, we included 30 pediatric patients who underwent prolonged MV and assessed the feasibility of measuring three diaphragmatic ultrasound indices (DE, DTF and TPIA) as well as lung ultrasound score during SBT to predict MV weaning success.

Clinically our data showed similar results to what was presented in some of the previous studies where MV duration was significantly longer in the weaning failure group [ 1 , 7 , 11 ] with other studies showed no significant correlation between MV duration and weaning success [ 10 , 12 , 13 , 14 ].

Regarding diaphragmatic US, DE was a significant predictor of weaning success in our study which agrees with most studies done in adults [ 9 ]. However, this is not the case in pediatric studies as only Abdel Rahman et al. [ 7 ] found significant association between DE and weaning outcome albeit only in Infants’ age group, while Xue et al. [ 1 ] found no significant correlation. Our DE cutoff values were different values than those of Abdel Rahman et al. [ 7 ]. However, their right DE cutoff value was 6.5 mm ours was 4.1 mm while their left DE cutoff value was 6.1 mm ours was 5.5 mm.

We did not find a significant correlation between DTF and weaning outcome. DTF significance in recent literature is controversial, while most adult studies consensus that it is a significant predictor [ 9 ], a recent large multicenter study found no association between DTF and weaning outcome [ 15 ]. While in pediatric studies the disagreement increases, as four earlier studies have found significant association [ 1 , 2 , 7 , 12 ] while another more recent four studies did not. [ 10 , 11 , 13 , 14 ]. The differences between the results of various studies could be attributed to multiple heterogenicities between them; first of which is the duration of the SBT and the exact time of acquiring the US measurement during it, where a longer SBT (As was imposed by our PICU team-up to 12 h) enables the diaphragm to regain its function before extubation. SBT duration by Xue et al. [ 1 ] was 30 min, by Abdel Rahman et al. [ 7 ] was 30–120 min and by Duyndam et al. [ 13 ] was 120 min, while the rest of the studies did not specify the exact duration of the SBT. Acquiring the US measurements at the end of a long SBT will lead to different measurements than acquiring it at the beginning. The second heterogenicity is caused by the difference in measurement technique, where some studies measured in B-mode and others measured in M-mode. Most studies were measured from the mid-point of the pleural echogenic line to the mid-point of the peritoneum echogenic line, while other studies were included only the hypoechoic muscle layer [ 1 , 10 ]. The prevailing agreement now suggests measuring only the muscle contained within the pleura and peritoneum, a perspective that was not available to us when we commenced our research. This is due to the biological activity of membranes, where mechanical forces associated with ventilation could potentially trigger inflammation, leading to tissue remodeling and thickening. Such tissue remodeling may have contributed to fluctuations in the size and thickness of the diaphragm [ 13 ]. Differences in the patient posture, sedation protocol and SBT ventilator settings are also a major source of heterogenicities between the studies.

It should be noted that all the studies that have found no significant association between DTF and weaning outcome have found significant association between MV and diaphragmatic atrophy as well as decrease in DTF, proving that VIDD is an entity that needs to be further investigated in how to measure it and prevent it [ 10 , 11 , 13 , 14 ].

TPIA was a parameter proposed by Theerawit et al. [ 6 ] in adults and has found that longer TPIA correlated with successful weaning. It had also strong association with RSBI, suggesting that TPIA could be an indicator for diaphragmatic strength. However, in our study we found no association between TPIA and weaning outcome. This could be attributed to the difference in SBT protocol as well as anatomical or physiological differences between adult and children that impact respiratory mechanics and the fact that weaning failure may be secondary to pathologies other than VIDD.

We were only able to measure DE and TPIA in 56.7% (17 out of 30) of the left diaphragms using the microconvex probe. This was due to inability to visualize the left diaphragm due to the smaller acoustic window offered by the spleen as compared to the liver on the right side and masking by intestinal gases. Nonetheless, we should state that we were able to visualize the left diaphragm motion in all patients by changing the probe position and placing it cranio-caudally in mid axillary or posterior axillary line, yet this will place the diaphragmatic motion at 90° to the US beam rendering M-mode ineffective in measuring the DE or TPIA. Most of the studies examined only the right diaphragm [ 1 , 2 , 10 , 11 , 12 , 13 , 14 ] depending on data from multiple previous studies, showing that there was significant difference regarding both sides in their US measurements [ 8 ]. Even so, we do recommend examining the left diaphragm in any available view primarily to exclude the absence of diaphragmatic motility or the presence of severe diaphragmatic dysfunction.

This study had multiple limitations. First of which is the smaller sample size that included all pediatric population. We do recommend further studies to include larger sample with stratification of pediatric population into infants, children and adolescent age groups. Secondly, we did not fix the time of US examination during our relatively long SBT which could have led to heterogeneous data. Finally, while diaphragm muscle strength is the focus of the current study, it is worth noting that diaphragmatic endurance also holds significance in the weaning from MV. Consequently, examining indicators like the diaphragmatic time-tension index alongside others could provide insights into how diaphragmatic endurance relates to the success of weaning.

We have found that DE is a predictor of weaning success while DTF and diaphragmatic TPIA had no correlation with weaning outcome. Further studies should be done using standardized weaning protocol and US examination time as well as investigate other measurements assessing diaphragmatic endurance.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

• Diaphragmatic excursion
• Diaphragmatic thickening fraction

Fraction of inspired oxygen

• Mechanical ventilation

Noninvasive ventilation

Partial pressure of arterial oxygen

Positive end-expiratory pressure

Pediatric intensive care unit

Rapid shallow breathing index

Spontaneous breathing trial

Time to peak inspiratory amplitude

Ventilator-induced diaphragmatic dysfunction

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Department of Diagnostic and Interventional Radiology, and Molecular Imaging, Ain Shams University, Faculty of Medicine, Ramsis St., Abbasia, Cairo, 11657, Egypt

Amir Maurice Eskander, Abeer Maghawry Abd-Elhameed, Noha Mohamed Osman & George Ezzat ElKess

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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by AME, AMA, NMO, SMM and GEE. The first draft of the manuscript was written by AME. The authors read and approved the final manuscript.

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Eskander, A.M., Abd-Elhameed, A.M., Osman, N.M. et al. Role of diaphragmatic ultrasound in predicting weaning success from mechanical ventilation in pediatric intensive care unit. Egypt J Radiol Nucl Med 55 , 114 (2024). https://doi.org/10.1186/s43055-024-01285-0

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Ultrasonographic Assessment of Diaphragmatic Excursion and its Correlation with Spirometry in Chronic Obstructive Pulmonary Disease Patients

Mahvish qaiser.

Department of Rehabilitation Sciences, SNSAH, Jamia Hamdard, India

Abhinav Jain

1 Department of Radiodiagnosis, Hamdard Institute of Medical Sciences and Research, New Delhi, India

Introduction:

Chronic obstructive pulmonary disease (COPD) is a common disease. Spirometry is a standard method of assessment of severity of COPD. We evaluate utility of diaphragmatic excursion using ultrasonography in COPD patients and compare this technique with spirometry.

Twenty-six COPD patients and 18 self-reported healthy controls were included in this study. After taking the sociodemographic data, measurement of diaphragm excursion was done using M-mode and B-mode ultrasound. Lung function was assessed by spirometry.

In the COPD group, diaphragmatic excursion was found to be reduced, and it correlates with forced expiratory volume in 1 s (FEV1)/forced vital capacity, whereas it did not correlate with FEV1.

Conclusion:

Ultrasound assessment of diaphragmatic excursion is an easy, noninvasive, and readily available diagnostic tool and correlates with spirometry in estimation of severity of COPD.

Introduction

Chronic obstructive pulmonary disease (COPD) is a common preventable and treatable disease as per the Global Initiative for Chronic Obstructive Lung Disease (GOLD) and is characterized by persistent respiratory symptoms and airflow limitation that is due to airway and/or alveolar abnormalities usually caused by significant exposure to noxious particles or gases.[ 1 ]

According to the GOLD report, COPD is projected to be the third leading cause of death by 2020, and currently, it is the fourth.[ 2 , 3 ] The Global Burden of Disease Study done in 2013 attributed COPD as the cause of death for >3 million people that constitutes 6% of all deaths globally.[ 2 ] A review of the published reports revealed 384 million cases of COPD in 2010 which is 11.7% globally.[ 4 ] This makes COPD a leading cause of morbidity and mortality, thus causing huge economic and social burden on the society.[ 3 , 5 ] As per the WHO estimates, 90% of COPD-related deaths occur in developing countries. India and China alone account for 66% of global COPD mortality which is approximately 33% of the total human population.[ 6 , 7 ]

COPD impairs the function of diaphragm muscle which is the primary muscle of inspiration. Diaphragm provides 75% of the increase in lung volume during quiet inspiration.[ 8 ] Movement of diaphragm during breathing is called diaphragm mobility. Movement of diaphragm from end-expiration to full inspiration is known as diaphragm excursion.

Diaphragmatic mobility has been found to be lower in patients with COPD than in healthy elderly individuals due to hyperinflated chest.[ 9 ] COPD patients with thoracic hyperkyphosis have lower diaphragm mobility than those without it. An increase in kyphosis angle decreases the diaphragmatic mobility.[ 10 ]

Ultrasonography is a cost-effective, radiation-free, widely available, and real-time investigation.[ 11 ] Many studies have proposed the possible use of ultrasonography to measure the diaphragmatic excursion.[ 11 , 12 , 13 , 14 ] Although, the literature is limited. Spirometry is a noninvasive, easy, and valid tool for COPD assessment. There are established criteria based on spirometry, according to which COPD can be classified as mild, moderate, severe, and very severe.[ 1 , 9 ] Our study evaluates the diaphragmatic excursion on the basis of preestablished protocols and compares the outcome with the spirometry results. This study explores a new opportunity of using standard ultrasonography as a tool to establish the diagnosis of COPD and assess the severity of the same.

Materials and Methods

The study was conducted between January and April 2020 at a tertiary care hospital. Forty-four study participants were recruited from chest OPD of our hospital after their due informed consent. Out of these, 26 were COPD patients who were labeled as study group and 18 were non-COPD patients who were labeled as control group. For the COPD group, only those patients who did not require oxygen supplementation and were clinically stable were recruited. Both smokers and nonsmokers were recruited in both the groups.

The exclusion criteria included any patient with recent COPD exacerbation in the last 3 months, patients with comorbidities such as cardiac disease, pulmonary fibrosis, or ankylosing spondylitis, or patients who were unable to understand and perform the test.

All these patients underwent spirometry and ultrasonographic assessment of diaphragmatic excursion on the same day as per the below-mentioned protocol. These patients and controls were randomized so that the spirometry observer and radiologist were blinded for the cases and controls.

All participants underwent a detailed postbronchodilator spirometry examination using a calibrated Spirolab III MIR Spirometer in sitting position. Spirometry was performed thrice by experienced technicians at our pulmonary function laboratory. Patients were asked to take a maximal inspiration and then to forcefully expel air for as long and as quickly as possible. Results were recorded and saved for statistical analyses.[ 15 ]

Ultrasonography

Ultrasound assessment of diaphragmatic excursion was done by experienced ultrasonologists. Diaphragmatic excursion for patients was measured on GE make, Voluson S8 series ultrasound machine. The assessment was done in supine position using M-mode and B-mode techniques in quiet and deep breathing scenarios. For M-mode assessment, the transducer was placed in the subcostal region at the midclavicular line with probe tilted cranially, and for B-mode assessment, patients were scanned by placing the transducer in the subcostal region at the midclavicular line with probe tilted horizontally[ 12 , 13 ] [ Figure 1 ]. Ultrasonologists were blinded about the spirometry results.

Ultrasound images on diaphragm (arrow). (a) M-Mode scan done at the midclavicular line to assess diaphragmatic motility. (b) B-Mode acquisition shown here as a still from cine-loop image obtained to measure diaphragmatic excursion

Sample size calculation

The sample size required for 40+ years of age group COPD in our district is 1,000,000 individuals which was calculated based on the assumption that the lowest prevalence of COPD in our district is about 4.75% with an absolute precision of 5%, CI of 80%, and design effect as 1.[ 6 , 15 , 16 ]

Sample size formula n = (DEFF * N*p*q]/[(d2/Z2 1-α/2* (N-1) +p*q].

Statistical analysis

Data was analyzed using IBM SPSS statistical package for Linux version 16.0. Bangalore, India. Demographic data were analyzed using independent samples t-test. Diaphragmatic excursion and lung function were analyzed by an independent t-test. To analyze the relationship between lung function and diaphragmatic excursion, Karl Pearson's correlation coefficient test was used. The level of significance was <0.05 ( P < 0.05).

Forty-eight participants were included in the study. Out of those, 30 were COPD and 18 were non-COPD. Four COPD patients were dropouts. Therefore, their data were not included in this study. Nineteen were male COPD and 11 were healthy male. The rest of them are females. Table 1 shows the mean and standard deviation of different variables in both the groups.

Mean and standard deviation data of study and control groups

FEV 1 : Forced expiratory volume in 1 s; FVC: Forced vital capacity, DE: Diaphragmatic excursion

Independent t -test between the groups revealed that diaphragmatic mobility and lung function are reduced in COPD patients than healthy controls with level of significance <0.01 ( P < 0.01).

Pearson's correlations between diaphragmatic excursion and lung measurements showed a positive strong correlation between forced expiratory volume in 1 s/forced vital capacity (FEV1/FVC) with M-mode ( r = 0.75) [ Table 2 and Figure 2 ] and B-mode ( r = 0.85) in the study group [ Table 3 and Figure 3 ], but this relationship was not found in control controls. There is a weak correlation between FEV1 and M-mode in the study group. There is a strong correlation between M-mode and FEV1 ( r = − 0.50) in the control group.

Relationship between diaphragmatic excursion (M-mode) and variables in study group

FEV 1 : Forced expiratory volume in 1 s; FVC: Forced vital capacity, SD: Standard deviation

Correlation between forced expiratory volume in 1 s/forced vital capacity and M-mode in study group

Relationship between diaphragmatic excursion (B-mode) and variables in study group

Correlation between forced expiratory volume in 1 s/forced vital capacity and B-mode in experimental group

Finally, we observed that diaphragmatic excursion was significantly reduced in the study group than controls ( P < 0.05). Spirometry measurements showed a significant difference between the groups. FEV1/FVC is significantly reduced in COPD [ Table 1 ].

The study establishes that COPD affects diaphragmatic excursion and lung function. We found that diaphragmatic excursion was reduced in COPD than controls. Decreased diaphragmatic excursion shows that contractile ability of diaphragm is reduced in COPD.

The reason of reduced contractility lies in the pathophysiology of the disease. COPD includes bronchitis and emphysema which cause airway obstruction and air trapping in the lungs. Normally, diaphragm moves caudally during inspiration and cranially during expiration. COPD can cause hyperinflation of the lungs, and therefore, diaphragm shifts caudally. This causes mechanical disadvantage of the diaphragm muscle.[ 1 ] Previous studies revealed that reduced diaphragmatic mobility is associated with increased perception of dyspnea. Structural changes cause flattening of the diaphragm which reduces their ability to move cranially and caudally.[ 9 , 10 , 12 ]

Another important outcome of this study is the correlation between sonographic assessment of diaphragmatic excursion and spirometry results. In the present study, we found that diaphragmatic excursion strongly correlates with FEV1/FVC and weakly correlates with FEV1 in the study group. These findings corroborate those of Rocha et al ., who found that diaphragmatic mobility is related to pulmonary parameters (FEV1, FEV1/FVC, FVC, IC, and MVV).[ 9 ] Progression of the disease causes shortening of diaphragm fibers and decreases resting diaphragm muscle length. This causes a decrease in their ventilator capacity and lung function.

COPD causes inflammation and obstruction of the airways that lead to air trapping in the alveoli. As the severity of the disease increases, lung function decreases. COPD can cause hyperkyphosis in later stage which reduces the expansion of the chest wall. A study proved that diaphragmatic mobility is correlated with kyphotic angle.[ 10 ] Hence we can say COPD affects diaphragmatic mobility and lung function.

The limitation of the present study is that only two Stage 4 COPD patients were involved because most of them came to chest OPD with acute exacerbation. Another limitation is that only right hemidiaphragm was assessed on ultrasonography.

Further studies with larger number of patients, especially with severe COPD (Stage 4), would be required covering wider geographical areas for standardized guidelines on assessment of diaphragmatic excursion in COPD patients.

This study describes the use of ultrasonography for assessing the diaphragmatic excursion. Sonographically determined diaphragmatic excursion strongly correlates with FEV1/FVC. Both the B-mode and M-mode approaches can be used to measure the diaphragmatic excursion, and these correlate well with the severity of COPD.

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Conflicts of interest.

There are no conflicts of interest.