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1 Department of Radiology, Assaf Harofeh Medical Center, Zerifin 70300 Israel; and Sackler Faculty of Medicine, Tel-Aviv University, Tel Aviv Israel
Received May 10, 1999;
accepted after revision June 29, 1999.
Address correspondence to S. Strauss.
Abstract
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SUBJECTS AND METHODS. Sonography of the neck was performed with a high-resolution linear array transducer to show the sides of the cricoid cartilage ring in both the sagittal and transverse planes. Twenty-three boys and 33 girls, who ranged in age from 6 to 17 years, were examined. Calcifications in the cartilage were characterized by number and size, distribution pattern, and side-to-side symmetry.
RESULTS. Calcifications were seen either as small echogenic, nonshadowing foci or as larger irregular, echogenic areas with acoustic shadowing. Calcifications were found in 19 of the 23 boys and 26 of the 33 girls. The earliest cases were in three 7-year-old children. The incidence and number of echogenic foci generally increased with age. Most calcifications were in the center of the cartilage or distributed diffusely throughout. Side-to-side comparison of the number, size, and distribution pattern of the calcifications showed considerable variation.
CONCLUSION. The sides of the cricoid cartilage ring could be seen on sonography in both the sagittal and transverse planes. Calcifications within the cartilage were readily shown and were found in children at an earlier age than previously reported.
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As part of the aging process, ossification and calcification take place in the various cartilages of the laryngeal skeleton. Current anatomy and radiology literature suggest that this process begins during the third decade of life 2, 3, 4] but, to our knowledge, calcification in cricoid cartilage has not been evaluated previously using sonography. The purpose of this study was to determine the pattern of calcification in cricoid cartilage in healthy children on sonography.
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Sagittal images of the cartilage on both sides of the neck were obtained with the transducer inclined medially to approximately 30°. The cricoid cartilage was identified as a round or oval structure adjacent to the upper part of the lobe of the thyroid gland. The cartilage was uniformly hypoechoic relative to the adjacent thyroid gland, except for a thin anechoic peripheral layer. In this projection, the cartilage was 1-2 cm in diameter, depending on the age of the child. In the transverse view, with the transducer placed in the midline of the neck, both sides of the cricoid cartilage were seen as thin (2-4 mm) echogenic layers draped over the sides of the infraglottic air column (Fig. 1A, Fig. 1B).
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Calcifications were seen as bright echogenic foci within the cartilage and were easily located on the two orthogonal views. The calcifications were characterized by number and size of foci, position within the cartilage, and side-to-side symmetry. For the purpose of comparison, the cricoid cartilage in five volunteers who were more than 50 years old was examined.
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Calcifications were usually uniform in size in each patient. In 39 of the 45 children with calcifications, these calcifications were characterized as bright, echogenic, nonshadowing foci of 1 mm in diameter (Fig. 2A, Fig. 2B). In the six other children, the calcifications were larger, measuring up to 10 mm in diameter, and cast acoustic shadows (Fig. 3). All cases of the larger calcifications were found in the 14- to 17-year-old group.
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The number of calcifications on each side was semiquantitatively estimated as more or less than three echogenic foci in a single plane. This analysis showed that the number of foci in each cartilage generally increased with age (Fig. 4A, Fig. 4B). Only two of the 12 children in the 6- to 9-year-old group had more than three echogenic foci counted on a single image. Children with larger calcifications tended to have fewer echogenic foci, which possibly resulted from coalescence of the foci into a larger unit.
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In all the children except five, the echogenic foci were either distributed in a diffuse pattern throughout the cartilage or localized to the center. Calcification confined to the periphery, which was seen generally in older children, tended to be larger and either irregular or curvilinear in shape (Fig. 5A, Fig. 5B). Side-to-side comparison of the number, size, and distribution pattern of the echogenic foci showed considerable variation (Fig. 6A, Fig. 6B). Of all the children with cartilage calcification, the echogenic foci were found bilaterally in 27 and unilaterally in 18. Unilateral calcification was confined to the right side in 16 of the 18 children. No relationship between the age of the child and the symmetry of the calcifications was seen.
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In the five volunteers who were more than 50 years old, the cricoid cartilage was found to be heavily calcified and the outline of the cartilage was poorly visualized because of acoustic shadowing (Fig. 7).
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The thyroid, cricoid cartilage, and greater part of the arytenoid cartilage consist of hyaline cartilage that undergoes calcification and ossification as part of the aging process. The terms "ossified" and "calcified" are often used synonymously, although calcification always precedes ossification when cartilage becomes transformed into bone [10]. In this study, the term "calcification" is used, although no histologic proof is available to decide whether the bright foci seen in the cricoid cartilage are the result of ossification or calcification.
There are scant reports in the literature concerning the use of sonography for examination of the larynx. Garel et al. [10] assessed the anatomy of the larynx in healthy infants and children up to the age of 15 years on sonography. These researchers reported that the cricoid cartilage appears as a round hypoechoic structure in the transverse plane. Raghavendra et al. [11] studied the sonographic anatomy of the larynx in adult volunteers. Their study, however, focused on the vocal cords, and images were obtained only in the transverse plane. In these reports, calcification in the laryngeal cartilages is not mentioned.
We are not aware of any report of the use of sonography to visualize the cricoid cartilage in the longitudinal view. This view is easily obtained using the upper pole of the thyroid gland as an acoustic window and scanning in a medially angled sagittal plane. Because of the homogeneously hypoechoic nature of the cricoid cartilage and the superior spatial resolution of high-frequency transducers, echogenic foci as small as 1 mm in diameter are readily displayed. These echogenic foci do not cast acoustic shadows, presumably because of their small size.
Based on radiographic and dissection findings, Keen and Wainright [12] reported that ossification on the right and left sides of the cricoid was equal and symmetric in extent. Jurik [7] used low-voltage radiography and found not only symmetric ossification of the cricoid, but also an unequal configuration of calcification on both sides. With only 48% of our cases showing calcifications in both the right and left sides, our findings agree with the CT findings of Yaeger et al. [8] that the process is asymmetric. We also found that the distribution and size of echogenic foci frequently differed between the two sides. The discrepancy in the literature, however, may be explained by the synonymous use of the terms calcification and ossification.
Comparing the sexes, Jurik [7] found calcification of the cricoid cartilage to be more marked and more frequent in females but the degree and frequency of ossification to be lower in females. Hately et al. [6] reported that the cricoid ossified similarly in both male and female patients. No significant sex differences emerged from our study.
We found that calcification of the cricoid cartilage increased with age but that there was no strict correlation between the two. The earliest cases of calcification were in two 7-year-old boys and one 7-year-old girl, but 21 (48%) of the 44 children in the 10- to 13-year-old and 14- to 17-year-old groups had no evidence of calcification in one side or both sides of the cricoid ring. This finding is in accordance with previous reports that differences between individuals belonging to the same age group may be considerable [6, 7, 12, 13]. A genetic factor to account for individual differences has been proposed by Vastine and Vastine [14]. They found the same pattern of calcification in the laryngeal cartilages in five pairs of identical twins.
There are two limitations of our study. First, the results account for calcifications only along the sides of the cricoid cartilage ring. Previous studies have shown that the calcification process usually starts in the posterior lamina and later spreads anteriorly along the arch [6, 7, 12]. It is therefore possible that if all parts of the cricoid cartilage could be visualized sonographically, calcification would be seen in the lamina in most, if not all, patients in whom it was seen along the sides of the ring. Second, histologic proof that the echogenic foci are indeed calcifications was not obtained. We are not aware, however, of any process other than calcification that could account for the echogenic foci, which were found in increasing numbers and size with advancing age. Histologic findings in a study of the ossification of the larynx were reported by Keen and Wainright [12]. They found that calcified foci that are unaccompanied by ossification may appear as early as the second decade. These foci of calcification may become confluent, forming plaques of calcium that can be regarded as precursors of ossification because the foci invariably disappear with the spread of ossification.
Congenital conditions causing premature calcification and acquired forms of premature calcification of the larynx are rare and present as stridor in infants and young children. Premature calcification is usually associated with tracheal or tracheobronchial calcification, and its cause is unknown [15, 16]. Although in this study we examined only healthy children, our method could potentially be used to assess the occurrence of laryngeal calcification in children with congenital conditions such as a chondrodysplasia punctata and Keutel syndrome; in children with acquired forms of premature cartilage calcification, such as warfarin embryopathy after long periods of warfarin therapy; and in children with idiopathic infantile hypercalcemia [17, 18].
The results of our study are important in cases in which children undergo radiographic examination for a foreign body embedded in the hypopharynx. Our findings show that cricoid cartilage calcification occurs earlier than previously reported; therefore, the possibility that it may masquerade as a foreign body should not be discounted in children [19].
In summary, the sides of the cricoid cartilage ring are easily visualized on sonography in both the sagittal and transverse planes. The cartilage has a homogeneous hypoechoic texture relative to the adjacent thyroid gland. Calcifications are readily displayed as bright, nonshadowing, small echogenic foci or as larger irregular echogenic areas that may cast acoustic shadows. Calcifications were found at an earlier age than previously reported.
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