Lakhal, Karim MD*; Delplace, Xavier MD*; Cottier, Jean-Philippe MD†; Tranquart, François MD‡; Sauvagnac, Xavier MD*; Mercier, Colette MD*; Fusciardi, Jacques MD*; Laffon, Marc MD*
From the *Groupement d’Anesthésie Réanimation, †Service de Neuroradiologie, and ‡Groupement d’Imagerie Médicale, CHU Tours, Tours, France.
Accepted for publication November 6, 2006.
Address correspondence and reprint requests to Karim Lakhal, Réanimation Médicale et Infectieuse., Hopital Bichat-Claude Bernard, 46 Ave Henri Huchard, 75018 Paris, France. Address e-mail to firstname.lastname@example.org.
BACKGROUND: In healthy patients, the narrowest diameter of the subglottic upper airway is the width of the air-column at the level of the cricoid cartilage. This diameter governs the selection of the endotracheal tube size, as excessive tube diameter may damage the tracheal mucosa leading to postextubation stridor or subglottic stenosis. Unfortunately, selecting endotracheal tube size based on height, weight, or age does not reliably lead to the proper tube. The knowledge of airway diameter, especially using a bedside noninvasive tool, could therefore be helpful in anesthesia and intensive care.
METHODS: We studied 19 healthy volunteers (27 ± 3 yr, nine females) to compare the transverse diameter of the cricoid lumen assessed by ultrasonography and magnetic resonance imaging.
RESULTS: We found a strong correlation between the two techniques (r = 0.99, P < 0.05) confirmed by Bland–Altman analysis with a bias of 0.14 mm, a precision of 0.33 mm, and limits of agreement of −0.68 mm/0.96 mm.
CONCLUSION: In young healthy adults, ultrasonography appeared to be a reliable tool to assess the diameter of the subglottic upper airway.
Endotracheal tubes (ETT) lead to complications such as airway edema or laryngotracheal stenosis. Because the smallest diameter of the normal upper airway is located at the level of the cricoid cartilage, these complications are often located in this area (1,2). The ETT may induce mucosal and cartilaginous ischemia because of an excessive size or an over-inflated cuff. The airway vulnerability in the cricoid area is not homogeneous because the transverse diameter is smaller than the anteroposterior diameter (3–5).
In anesthesia and intensive care, assessment of the upper airway’s narrowest diameter may be helpful to select the ETT size and also to assess laryngeal stenosis after prolonged tracheal intubation. The smallest diameter cannot be reliably predicted by height or weight, especially in adults (2,6). Ultrasonography is an appealing noninvasive technique for this purpose. Among adults (7) and children (8), the transverse diameter of the trachea in the neck can be visualized by ultrasound. In contrast the anteroposterior diameter cannot be assessed, because the acoustic shadow generated by the air column obscures the location of the posterior wall. Morphometric measurements performed in animals have confirmed that laryngeal lumen measurements by ultrasound are reliable (9,10).
Our objective was to compare, in healthy subjects, transverse airway diameter in the cricoid area assessed by ultrasonography to assessment by magnetic resonance imaging (MRI).
After local ethics committee approval and informed consent, 19 healthy volunteers (nine females) were studied. Exclusion criteria included preexisting laryngeal pathology or contraindication to MRI imaging. Each subject underwent both an MRI and ultrasonography of the cricoid area, performed by two independent operators. The echographer had been trained by performing 15 laryngeal ultrasonographical examinations before the beginning of the study.
The measurements were performed in the supine position, with the head in slight extension. To avoid respiratory-induced changes in upper airway dimensions, subjects were instructed to take a slow inspiration at constant flow during the measurement period.
MRIs were obtained with standard T1-weighted spin-echo sequences with a 1,5 T system (Signa, GE Medical Systems, Milwaukee, WI) using a neck coil. Acquisitions were initially performed in the sagittal and coronal planes to generate images of the cricoid cartilage in the transverse plane (TE, 4.2 m; TR, 11.8 m; matrix size 256 × 160; section thickness 4 mm). To get high-resolution images during an inspiratory maneuver, acquisition time was set at 7 s. The resolution in plane was 0.625 mm (y axis) × 1 mm (x axis).
Ultrasonography measurements were performed in B-mode (Acuson 128 XP, Siemens, Mountain View, CA) with a linear probe (40 mm length, frequencies 7–15 MHz) placed on the midline of the anterior neck. To avoid any confusion between the cricoid cartilage and a tracheal ring, the ultrasonography procedure began with the location of the true vocal folds (paired hyperechoic linear structures with respiratory and swallowing mobility). Then the probe was moved caudally to visualize the cricoid arch (Fig. 1).
With both techniques, the transverse air-column diameter was measured at the cephalic half of the cricoid cartilage which is narrower than the caudal part (4,6). The anteroposterior diameter, at the same level, was only measured with MRI.
The Bland–Altman method (11) and linear regression were used to compare the transverse diameters measured by the two techniques in each subject. A paired Wilcoxon test was used to compare MRI cricoid transverse and anteroposterior diameters. A P value <0.05 was considered significant. Results were expressed as mean diameter ± sd.
The 19 subjects (27 ± 3 yr) underwent ultrasonography and MRI without technical difficulties. The ultrasonography procedure never exceeded 5 min. Measurements were performed adequately in all patients.
Bland–Altman analysis of the ultrasound and MRI measurements of the transverse cricoid lumen diameter noted a bias of 0.14 mm with a precision of 0.33 mm. The limits of agreement were −0.68 mm/0.96 mm (Fig. 2).
There was a strong correlation between ultrasonography and MRI measurements of the transverse diameter (n = 19, r = 0.99, P < 0.05).
MRI measurements indicated that the cricoid lumen transverse diameter (15 ± 2 mm) was smaller than that of the anteroposterior (19 ± 3 mm; P < 0.05).
Our results show that ultrasonography allows measurements of the air-column width at the level of the cricoid cartilage with a precision of 0.33 mm. They also confirm that in vivo the transverse diameter is smaller than the anteroposterior diameter. These results suggest that ultrasonography is useful to assess subglottic diameter in the clinical setting (9). The ease of using ultrasound is reinforced by the need for only 15 training examinations for nonskilled physicians to perform these measurements.
The assessment of laryngeal dimensions is usually performed noninvasively by computed tomography scan or MRI, or invasively by endoscopy or the ETT sizing method (5). Most studies used the ETT sizing technique in anesthetized patients to measure the smallest laryngeal diameter (12), seeking the tube size that allowed an audible air leak for insufflating pressures between 10 and 25 cm H2O. This technique has a low precision because the ETT outer diameter increases only by 0.6–0.8 mm and because the pressure threshold allowing an audible air leak around the ETT may vary either with the depth of neuromuscular blockade or the head flexion (13) or subjective physician assessment (14). Moreover, the measure may be overestimated because the shape of the subglottic area is frequently uncylindrical which variably increases the air leak. The measure may also be underestimated by successive ETT replacements if laryngeal edema occurs (15). MRI provides high-quality laryngeal images permitting accurate measurements of the larynx (16) and can be considered a noninvasive gold standard method in vivo. Laryngeal ultrasonography was proposed to examine the larynx in infants, children (8) and adults (7,17). This bedside tool does not require strict immobility, especially in infants, as opposed to MRI or computed tomography scan, for which infants are often anesthetized and intubated. In this case, the ETT required for anesthesia may deform the laryngeal structures and therefore disturb the measurements. Ultrasonography is an operator-dependent technique; however, it is relatively simple to learn. Only 15 procedures were required for the operator to obtain reliable and reproducible measurements.
The age-dependent physiologic calcification of the larynx creates an acoustic shadow. This laryngeal calcification usually starts in adults at the age of approximately 30 yr and may sometimes even be present during teenage years (18). Among our young adult subjects, calcifications of the cricoid arch did not disturb our measurement, because the shadow was small or easily avoidable. However, these calcifications may constitute an important limitation of laryngeal ultrasonography in older patients.
The good agreement of the ultrasonography method to measure the smallest subglottic diameter demonstrated in our study was not in accord with findings by Husein et al. (10). In their study, which included nine patients aged 1–20 yr, ultrasonography was compared withthe ETT sizing method. They noted that ultrasonography was unable to provide accurate measurement of the subglottic diameters. The ETT sizing method, contrary to MRI which permits a direct measure, is not the gold standard method. The limitations in method that we previously noted easily explain the difference of their conclusion.
Our results suggested that ultrasonography may help to select the proper ETT size. This is particularly significant in infants and children. Unfortunately because we needed the subjects’ collaboration for the slow inspiration maneuver in MRI, we did not include this population in our study. However, because laryngeal cartilage calcification is rare in this population, and anatomic subglottis differences with adults are minimal, ultrasonography could likely be used in pediatrics (5). To choose the ETT size, many formulas (including age, weight, height) have been proposed for infants and children. Most formulas were established using the ETT sizing technique (19). Ultrasonography could assess the accuracy of the formulas in a prospective study on true morphometric measurements.
Our study did not included any patient with a laryngeal pathology. Our findings indicate that a similar study in these patients is necessary. Ultrasound may be useful to evaluate patients with subglottic stenosis, a common disorder in neonatal or pediatric anesthesia and intensive care (20–22). Proper ETT selection is important for patients with a history of tracheostomy who present for procedures which require intubation. Ultrasound assessment of the airway in these patients could facilitate the diagnosis, classification and follow-up of their pathology, as well as guide ETT size selection (15).
Our study validates the reliability of ultrasound to measure subglottic diameter in healthy subjects and thus provides the basis for further development of these potential applications.
In healthy young adults, ultrasonography is a reliable tool to assess the smallest diameter of the cricoid lumen, i.e., its transverse diameter, allowing noninvasive bedside assessment of the upper airway. Further studies are necessary in children and also in patients with subglottic stenosis.
We are grateful to Mrs. Ribeyrolles Catherine for editorial assistance.
1. Donnelly WH. Histopathology of endotracheal intubation. An autopsy study of 99 cases. Arch Pathol 1969;88:511–20.
2. Seymour AH, Prakash N. A cadaver study to measure the adult glottis and subglottis: defining a problem associated with the use of double-lumen tubes. J Cardiothorac Vasc Anesth 2002;16:196–8.
3. Litman RS, Weissend EE, Shibata D, Westesson PL. Developmental changes of laryngeal dimensions in unparalyzed, sedated children. Anesthesiology 2003;98:41–5.
4. Eckel HE, Sittel C, Zorowka P, Jerke A. Dimensions of the laryngeal framework in adults. Surg Radiol Anat 1994;16:31–6.
5. Hudgins PA, Siegel J, Jacobs I, Abramowsky CR. The normal pediatric larynx on CT and MR. AJNR Am J Neuroradiol 1997;18:239–45.
6. Randestad A, Lindholm CE, Fabian P. Dimensions of the cricoid cartilage and the trachea. Laryngoscope 2000;110:1957–61.
7. Carp H, Bundy A. A preliminary study of the ultrasound examination of the vocal cords and larynx. Anesth Analg 1992;75:639–40.
8. Garel C, Contencin P, Polonovski JM, et al. Laryngeal ultrasonography in infants and children: a new way of investigating. Normal and pathological findings. Int J Pediatr Otorhinolaryngol 1992;23:107–15.
9. Giguere CM, Manoukian JJ, Patenaude Y, Platt R. Ultrasound and a new videobronchoscopic technique to measure the subglottic diameter. J Otolaryngol 2000;29:290–8.
10. Husein M, Manoukian JJ, Platt R, et al. Ultrasonography and videobronchoscopy to assess the subglottic diameter in the paediatric population: a first look. J Otolaryngol 2002;31:220–6.
11. Bland JM, Altman DG. Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1986;1:307–10.
12. Cotton RT, Gray SD, Miller RP. Update of the Cincinnati experience in pediatric laryngotracheal reconstruction. Laryngoscope 1989;99:1111–6.
13. Finholt DA, Henry DB, Raphaely RC. Factors affecting leak around tracheal tubes in children. Can Anaesth Soc J 1985;32:326–9.
14. Schwartz RE, Stayer SA, Pasquariello CA. Tracheal tube leak test—is there inter-observer agreement? Can J Anaesth 1993;40:1049–52.
15. Myer CM III, O’Connor DM, Cotton RT. Proposed grading system for subglottic stenosis based on endotracheal tube sizes. Ann Otol Rhinol Laryngol 1994;103:319–23.
16. Bertolani M, Calandra Buonaura P, Spina V, et al. [Spin-echo anatomy of the larynx in MRI at 1.5 T]. J Radiol 1993;74:1–12.
17. Ding LW, Wang HC, Wu HD, et al. Laryngeal ultrasound: a useful method in predicting post-extubation stridor. A pilot study. Eur Respir J 2006;27:384–9.
18. Strauss S. Sonographic appearance of cricoid cartilage calcification in healthy children. AJR Am J Roentgenol 2000;174:223–8.
19. Cole F. Pediatric formulas for the anesthesiologist. AMA J Dis Child 1957;94:672–3.
20. Eckenhoff JE. Some anatomic considerations of the infant larynx influencing endotracheal anesthesia. Anesthesiology 1951;12:401–10.
21. Benjamin B. Prolonged intubation injuries of the larynx: endoscopic diagnosis, classification, and treatment. Ann Otol Rhinol Laryngol Suppl 1993;160:1–15.
22. Wiel E, Vilette B, Darras JA, et al. Laryngotracheal stenosis in children after intubation. Report of five cases. Paediatr Anaesth 1997;7:415–9.