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Portable ultrasound has resulted in the creation of clinical protocols for rapid bedside diagnosis and interventions, commonly referred to as point-of-care ultrasound (POCUS). In pediatric perioperative care, POCUS allows evaluation of basic physiological functions and assessment of the clinical patient status. The majority of critical incidences in pediatric anesthesia are airway-related, but the role of ultrasound in pediatric airway management has not yet been fully explored. This narrative review discusses a structured airway examination to facilitate pediatric airway management. In addition, it explores how ultrasound examinations can be implemented into a pediatric airway POCUS algorithm.
Background
The increasing presence of ultrasound (US) machines in operating theaters, largely driven by advancements in regional anesthesia, has created an environment that is well-suited for airway ultrasound examinations. Several studies in both adults and children have highlighted the usefulness of ultrasonography in various areas of airway management, more specifically in determining endotracheal tube size and guiding tracheal placement and positioning [1‐3, 23]. Studies are also currently being conducted aiming at evaluating if ultrasonography can be used to predict difficult direct laryngoscopy, diagnose obstructive sleep apnea, and optimize the placement of supraglottic airway devices. In addition, recent publications have investigated its role in correctly identifying structures needed for surgical front of neck access [25]. Consistent with other POCUS concepts, however, each specific airway US investigation ideally requires standardization to be integrated into a comprehensive airway POCUS algorithm.
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Ultrasound machines emit high-frequency sound waves that penetrate tissues and encounter different interfaces within the airway. These sound waves either reflect or scatter depending on the acoustic impedance of the tissues. The returning waves are captured by the ultrasound probe, processed, and converted into real-time images. It is important to remember that the actual air in airways and lungs has a low acoustic impedance, i.e., it is difficult to use for imaging alone. The surrounding tissues, however, generally have higher acoustic impedance. The border zone between tissue and air thus creates strong reflections and artifacts, used to interpret the image obtained. Specific equipment required for pediatric airway ultrasound usually involves a high-frequency linear ultrasound probe, typically ranging from 6 to 15 MHz with good resolution but less penetration depth. The use of the smaller linear probe “hockey stick” might be necessary for young and small patients (Fig. 1) due to the lack of space for the use of the regular linear probe.
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Preparation and sizing of the airway
Airway ultrasound has emerged as a potentially valuable tool for predicting difficult intubation in children using the hyomental distance (HMD), an objective measure to determine neck extension [12]. The HMD appears to be promising tool for predicting difficult intubation even if the evidence is currently restricted mainly to children between 5 and 8 years old [29].
Integrating ultrasound findings with clinical assessment may enhance the preoperative airway evaluation and aid decision-making regarding the most appropriate airway management approach; however, further validation is required to establish standardized protocols and determine the optimal ultrasound parameters for predicting difficult intubation in pediatric populations. The usefulness as a standard part of a pediatric airway POCUS algorithm is thus currently not clear, even if images in cooperative children are relatively easy to obtain. Figure 2 shows an example of a scan highlighting features associated with preoperative airway evaluation.
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The rationale behind selecting the appropriate size of an endotracheal tube in pediatric patients is based on the potential adverse effects of incorrect tube selection and minimizing the number of intubation attempts, a known risk factor for adverse respiratory events in children [8, 11]. The use of too large tracheal tubes may result in airway trauma and edema [11], whereas smaller endotracheal tubes may lead to inadequate ventilation and increased airway resistance.
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Ultrasonography can be used to measure the subglottic diameter as a surrogate measure for appropriate endotracheal tube outer diameter size. Several studies have demonstrated better accuracy than traditional age-based formulas in selecting both cuffed and uncuffed tubes [3, 19, 20]. The outer diameter of the endotracheal tube at the subglottic level has been shown to correlate well with the diameter stated by the manufacturer [13]. In general, ultrasound-guided endotracheal tube selection using the subglottic transverse diameter as the benchmark has been shown to yield a success rate of between 60% and 90%, which is comparable to age-based and height-based formulas [3]. This approach, however, requires training, with an apparent learning curve which will limit the immediate usefulness of this technique [18].
It is important to mention that most of these studies classify successful choice of endotracheal tube based on the occurrence of “optimal fit”, a concept that is poorly defined and may be hampered by interobserver variability [21]. In addition, measurements were taken during apnea ignoring potential effects of airway pressure changes. Testing for optimal fit in the presence of continuous airway pressure demonstrated an optimal agreement between measurements and best-fit tubes when utilizing 15 cmH2O of continuous pressure and at the cricoid level [19]. With the now fully established use of cuffed endotracheal tubes, the definition of optimal fit may be of slightly less importance as cuffed tubes usually enable an adequate seal.
Therefore, the use of ultrasonography for endotracheal tube selection should ideally be performed with the patient lying supine, neck in mild extension, and a high-frequency linear probe placed transverse across the neck, with a face mask delivering 15 cmH2O continuous airway pressure. The transverse diameter measurement should be taken at the subglottic/cricoid level and verified with the outer diameter of available tubes in the operating room to guide tube selection (Fig. 3).
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Confirming endotracheal tube placement and assessment of insertion depth
Ultrasound imaging of the airway can serve as an effective tool for assessing tracheal intubation and guide insertion depth. Even if ultrasonography currently cannot replace the gold standard of capnography, it may be useful in situations with low cardiac output and peri-arrest where end-tidal carbon dioxide may be unreliable. Several methods for confirming successful intubation have been investigated and are described below.
Using ultrasonography to guide intubation can be done by direct visualization of the tube passing through vocal cords via several indirect measures. The most frequently reported technique is based on transverse ultrasound imaging of the anterior neck during intubation. The passage of an endotracheal tube through vocal cords will appear as a flutter disturbance of the image when the hyperechoic endotracheal tube passes through the cords. This, however, appears to be a relatively uncertain sign, and hence ultrasonography has instead been used to guide intubation indirectly by excluding esophageal intubation. Esophageal intubation can be seen as a classical “double trachea” sign, indicating esophageal position of the endotracheal tube. In certain patients, the esophagus can be visualized in a cervical transverse image, posterior (deeper) to the trachea (Fig. 4; [15]). Even if ultrasound-guided intubation appears useful in certain specific situations, currently, no large studies exist defining the accuracy of ultrasonography to exclude esophageal intubation; however, the use of ultrasonography to guide intubation should be weighed against the apparent advantages of video laryngoscopy, particularly in smaller children, where video laryngoscopy has been shown to be superior to traditional laryngoscopy [10].
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An alternative way of assessing endotracheal tube position and subsequent ventilation of both lungs is the documentation of the lung sliding sign. Lung sliding is the ultrasonographic representation of periodic movement between the visceral and parietal pleura during lung ventilation. It is more accurate than auscultation for confirming optimal tube location in children under 2 years of age, and thus a promising use of ultrasonography to confirm bilateral lung ventilation [2]. Protocols incorporating a cervical scan for the absence of a double trachea sign and thoracic bilateral lung sliding have been evaluated in both children and adults and may be incorporated into an airway POCUS protocol [15].
As direct visualization of the tube passing through vocal cords is a rather uncertain sign of adequate intubation, alternative methods aimed at enhancing the ultrasonic properties of an endotracheal tube have been suggested. Saline-filled cuffs have been used to visualize the endotracheal tube within the trachea (Fig. 5a). This allows the assessment of deeper structures with better precision, otherwise obscured by the acoustic shadowing of the trachea itself [22]. At the level of the suprasternal notch, the visualization of a cuff has been reported to be successful between 95–98% when compared to fiberoptic bronchoscopy and fluoroscopy [22, 24]. A promising expansion of this concept involves using the sagittal long-axis plane to assess the proximal border of the cuff when filled with saline [27]. This technique allows clinicians to ensure that the cuff is fully inserted below the level of the cricoid ring, reducing the risk of damage to narrower structures in the airway, such as the subglottic and cricoid cartilage (Fig. 5b; [26]).
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In addition to confirmation of tracheal placement, ultrasonography can also be used to determine the actual endotracheal tube insertion depth in relation to the carina, that has so far only been possible using radiological methods or fiberoptic visualization. For small patients, a linear or a curvilinear probe can be used on the parasternal area or suprasternal region to identify the aortic arch, which usually is in proximity to the right pulmonary artery (RPA) [2, 7]. The RPA is normally located at the level of the carina, and thus analyzing the distance between the tube tip and RPA will give a reasonable estimate of tube depth, usually aiming at 0.5–1.5 cm of distance in the neutral heal position (Fig. 6). A recent meta-analysis of 14 studies comparing ultrasound to other methods for assessing intubation depth in neonates demonstrated that ultrasound was able to visualize the endotracheal tube in 96.8% of examinations performed and had a pooled sensitivity of 93.4% in detecting appropriate tube positioning when compared to chest X‑ray. The distance to the carina revealed large limits of agreement however (± 0.75 cm), demonstrating a relative uncertainty when applying this strategy for endotracheal tube depth determination [7]. In larger patients, a midline longitudinal scan with a linear probe can detect a saline-filled cuff inside the trachea below the level of the cricoid cartilage. A transverse scan at the level of the suprasternal notch serves as a surrogate for proper tube level if a cuff with saline is used.
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Special situations
Selective bronchial intubation and lung isolation
The use of ultrasonography to guide adequate tip positioning also makes the method potentially useful to facilitate lung isolation. The demands for one-lung ventilation (OLV) in neonates and young children are increasing partially owing to the increasing use of video-assisted thoracoscopic surgery (VATS) [4]. The gold standard for assessment of lung isolation via bronchial blocker is fiberoptic assistance; however, ultrasonography is a valuable alternative tool, albeit with limitations [28]. The usefulness of ultrasonography is again confirming bilateral ventilation through the visualization of lung sliding in the ventilated lung and the lack of lung sliding in the non-ventilated side. The motion mode (M-mode) can also be utilized and will show the classical bar-code sign on the non-ventilated side, whereas the seashore sign will be easily seen in this mode in the ventilated lung (Fig. 7).
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Ultrasonography for front of neck access
Emergency front of neck access as a last resort in a “can’t intubate, can’t oxygenate” scenario is extremely rare in pediatric airway management [8]. There is limited evidence to support for the use of ultrasonography-guided “front of neck access” in infants. Front of neck access in infants and small children is technically challenging and requires regular and extensive training [23]. The provider must be able to identify the critical components of the airway anatomy to perform invasive procedures. Ultrasonography allows the anesthesiologist to electively identify and mark these critical structures prior to surgical airway procedures. Accuracy in locating the cricothyroid membrane in pediatric patients has been reported to be similar to measurements made with magnetic resonance imaging [25]. Ideally, ultrasonography should be used in combination with manual palpation to correctly identify key structures prior to incision. Figure 8 shows an example of a US view presenting the surgical landmarks for invasive airway access, a scan performed longitudinally in the midline of the neck.
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Airway pathologies
Airway ultrasonography has the potential to be incorporated into the examination of patients presenting with stridor or other suspected laryngeal pathologies [16]. Recent studies have reported that laryngeal ultrasonography is an effective method for diagnosing vocal cord paresis following aortic arch surgery in neonates and infants, comparable to naso-endoscopy [14]. Moreover, the US examination had less impact on the physiological stability, as judged by standard hemodynamic monitoring, which may be beneficial when handling small and fragile patients [17]. The examination has also been proposed as a screening tool for laryngomalacia in patients presenting with congenital stridor as well as a tool for evaluating abnormal airways of patients who had undergone previous reconstructions [5, 9]. It remains unclear to what extent this method can substitute fiberoptic inspection.
There is increasing evidence that measurements taken with ultrasonography correlate with the severity of obstructive sleep apnea (OSA) in the pediatric population by relating lateral pharyngeal wall thickness as well as total neck thickness at the retropharyngeal level [6]. These results can potentially be utilized when planning postoperative care.
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Pediatric airway point of care ultrasound (POCUS)
The routine use of ultrasonography in airway management cannot be recommended yet due to the relative lack of clinical studies aimed at comparing US to other alternative methods; however, a structured pediatric airway point of care ultrasound (POCUS) algorithm for the established airway ultrasound examinations may still be proposed based on the current evidence.
In any establishment of a POCUS algorithm, several additional aspects need to be considered. Ultrasound examinations are operator-dependent, even if standardized scoring regimens are used. This may potentially misguide diagnosis and treatment. In addition, as with most POCUS algorithms, the scientific data supporting the benefits compared to other objective imaging modalities should be taken into consideration. Figure 9 shows an example of such an algorithm.
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Even if the application of pediatric airway ultrasonography appears promising in many ways, it still faces several challenges before it can be established in routine practice. Many of the applicable examination points already have readily available gold standard methods. The use of ultrasonography in assisting with intubation may be challenging to justify in the era of video laryngoscopy, for example; however, pediatric airway ultrasound is a useful adjunct to existing pediatric airway assessment methods and a valuable learning opportunity for ultrasonography. Lastly, as with all ultrasonography algorithms, care should be taken not to lose focus of the physiological status of the actual patient.
Clinical practice
The current evidence for routine use of ultrasound in pediatric airway management is currently limited even if certain specific investigations are relatively well supported.
Incorporating specific pediatric airway ultrasound examinations into a comprehensive algorithm for pediatric airway management may help improve patient care, potentially reduce complications, and ensure a successful intubation and correct endotracheal tube placement.
Pediatric airway ultrasound requires proper training and expertise and should be used as a complementary tool to other established methods of airway evaluation.
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Declarations
Conflict of interest
L. Guimarães Ferreira Fonseca, G. Bertolizio, T. Engelhardt and J. Karlsson declare that they have no competing interests.
For this article no studies with human participants or animals were performed by any of the authors. All studies mentioned were in accordance with the ethical standards indicated in each case.
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
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