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Age-related changes affecting the cricoarytenoid joint seen on computed tomography.

Abstract

We conducted a retrospective chart review to compare four characteristics--cricoarytenoid joint ankylosis, narrowing, erosion, and density increases--in patients younger and older than 65 years. Our study population was made up of 100 patients, who were divided into two groups on the basis of age. The younger group (<65 yr) comprised 49 patients (27 men and 22 women), and the older group ([greater than or equal to] 65 yr) was made up of 51 patients (25 men and26 women). Findings on computed tomography (CT) of the neck were used to determine whether each of the four characteristics was present or absent. Overall, we found only one statistically significant difference between the two groups: ankylosis was significantly more common in the older group (p = 0.036). When we looked further at the side of these anatomic changes, we found that the older group had significantly more right-sided and left-sided ankylosis than did the younger group (p = 0.026 for both), as well as significantly more left-sided narrowing (p = 0.028) (some patients had bilateral involvement). When we analyzed age as a continuous variable, older age was again associated with significantly more ankylosis (p = 0.047) and narrowing (p = 0.011). We conclude that CT can be useful for assessing radiologic changes in the cricoarytenoid joint in elderly patients during the workup of dysphonia and abnormal movement of the vocal folds.

Introduction

With age, many changes affect the laryngeal structures; among them are the cricoarytenoid joints. These diarthrodial joints are formed by the articular facets of both the cricoid and arytenoid cartilages apposed in a multiaxial form. (1) In the elderly--which for the purposes of this study we defined as those aged 65 years and older--the articulation begins eroding and the perichondrium becomes thicker, which affects the precise movement of the arytenoid cartilages over the cricoid cartilage and alters the position of the vocal folds during phonation. These histologic and structural changes result in a change in voice quality. (2-4)

Among the different laryngeal imaging modalities, computed tomography (CT) is the best for assessing the cricoarytenoid joint. With its rapid image acquisition and low susceptibility to artifact induced by breathing and swallowing, it is considered by many to be the standard diagnostic imaging study for the evaluation of organic voice disorders. (5) Modern CT scanners allow for a reconstruction of high-quality images in multiple planes and orientations, and they provide excellent spatial resolution. (5)

While numerous reports have been published on the acoustic changes and voice symptoms often experienced by patients with presbyphonia, we found only two studies in the English-language literature that have described CT changes in the cricoarytenoid joint brought about by aging. (6,7) To the best of our knowledge, no other radiologic study has examined age-related changes affecting the cricoarytenoid joint using CT. In this article, we describe what we believe is only the third study of radiologic changes at the level of the cricoarytenoid joint as they relate to age.

Patients and methods

We retrospectively reviewed the charts of all patients who underwent CT of the neck at our medical center from July 2015 through March 2016. After excluding patients with rheumatologic disease, vocal fold paralysis, laryngeal lesions, and a history of laryngeal cancer, laryngeal surgery, or irradiation, our study population was made up of 100 patients.

We analyzed this population on the basis of age, using 65 years as the cutoff threshold. A total of 49 patients (27 men and 22 women) were younger than 65 years and 51 (25 men and 26 women) were aged 65 or older. There were no significant differences between the two groups in the overall number of patients in each group or the number of men and women in each group.

Axial, coronal, and sagittal CT images of the neck were obtained on a 64-slice machine (SOM ATOM Sensation 64; Siemens; Erlangen, Germany). The images were displayed at a window level of 150 Hounsfield units (HU) and a width of 650 HU to optimize the evaluation of the cartilage and surrounding soft tissues. The scans were reviewed by an experienced radiologist, who made anatomic measurements at the level of the cricoarytenoid joint to determine the presence and degree of ankylosis, narrowing, erosion, and density changes.

A normal-appearing cricoarytenoid joint was defined as one with a clearly visible soft-tissue plane between the articular surface of the cricoid cartilage and the surface of the arytenoid cartilage on two or more orthogonal planes, with homogeneous density of the cartilage (figure 1).

Ankylosis was defined as a complete fusion of the joint secondary to severe joint space narrowing, which was defined as the loss of the radiolucent intercartilaginous space between the cricoid and arytenoid cartilages (figure 2). Erosion was defined as the destruction of the articular cartilage at its surface (figure 3). Finally, density changes were defined as areas of increased density, particularly calcification at the articular surface of the cricoarytenoid joint (figure 4).

These four variables were classified as either present or absent. Because the cricoarytenoid joint is a multiaxial joint and cannot be completely visualized in a single slice, the presence of any variable needed to be identified on two or more planes.

Statistical analysis. Statistical analysis was performed with the Statistical Package for the Social Sciences software (v. 23). The association between age group and each variable was examined with the chi-square test and the Fisher exact test (for expected counts <5), and p values were reported.

Further analysis was conducted to examine associations according to which side of the neck was affected. Finally, age was also studied as a continuous measure. With the age distribution significantly deviating from normality (p <0.05; Shapiro-Wilktest), the nonparametric Mann-Whitney U test was used to examine the differences in median age between the two groups in terms of whether findings were present or absent. A p value of <0.05 was considered significant.

Ethical considerations. Before the initiation of our analysis, the study protocol was approved by the Institutional Review Board of the American University at Beirut Medical Center.

Results

The prevalence of cricoarytenoid joint ankylosis was significantly higher in the older group (p = 0.036). Joint narrowing was more common in the older group, but the difference did not reach statistical significance (p = 0.112). Only a slightly greater prevalence of joint erosion and increased density was seen in the older group (table 1).

With respect to the side of diagnosis (some patients exhibited bilateral involvement), the only significant difference on the right side was the presence of ankylosis, which was more prevalent in the older group (p = 0.026). On the left side, the older group had significantly more ankylosis (p = 0.026) and narrowing (p = 0.028) (table 2).

When age was taken as a continuous variable, the mean age of patients with ankylosis and narrowing was significantly higher than the age of those in whom these variables were absent (table 3).

Discussion

The laryngeal cartilage is of the hyaline type, and its ossification process begins around the age of 20 years; it occurs secondary to the progressive replacement of the cartilaginous tissue by lamellar bone and hematopoietic tissue. (3) In elderly patients, the perichondrium of the cricoid and arytenoid cartilages becomes thicker, as the formation of cartilaginous fibrillations can be seen on light microscopy. (8)

Furthermore, the cricoarytenoid joint exhibits erosion and roughening of its surfaces, which worsen progressively as the formation of chondrocyte clusters leads to exposure of the collagenous fibers. (8-10) These changes, along with a decrease in the adherent properties of the joint capsule, affect the precise movement of the arytenoid cartilage over the cricoid cartilage, which in turn ultimately affects vocal fold movement and quality of voice. (4,11)

CT is frequently used for laryngeal imaging. As previously mentioned, CT changes in the cricoarytenoid joint with age were previously looked at in two studies, but both carried some limitations. (6,7) In 1982, Yeager et al published a cadaveric study of 30 adult larynges. (6) Specimens had been obtained from 16 men and 14 women, all of whom were 50 years of age or older. The authors looked at patterns of ossification in the cricoarytenoid joint on CT. Twenty-one of 32 cricoarytenoid joint specimens showed a complete ossification of the vocal process, and 23 of 31 specimens exhibited some ossification of the arytenoid body.

As for the cricoid cartilage, their study found a difference in ossification between the inner and outer surfaces in the male donors; complete ossification was present on the inner surface in 12 specimens and on the outer surface in only 7. (6) Less ossification was seen at the level of the cricoid arch. No correlation was found between patterns of ossification and age. In addition, the pattern of ossification was more prominent on the left side than on the right, which led the authors to conclude that patterns of ossification are mainly asymmetric. No other radiologic features of the cricoarytenoid joint were looked at in this study.

A few years later, Cerat et al reported their histologic and radiologic examination of 8 cadaveric larynges using 1.5-mm contiguous CT slices. (7) They described the radiologic appearances of the cricoarytenoid joints as being either radiolucent or radiopaque. In 2 cases, the cricoid and arytenoid cartilages lacked calcification and were not visible. In addition, the cricoarytenoid joint could not be assessed in 3 other cases because the cartilages had not mineralized enough. In the 3 remaining cases, the cricoarytenoid joint was either radiolucent or radiopaque whenever the cricoid and arytenoid cartilages were overlapping.

The Cerat study was limited because only axial views were used to assess the cricoarytenoid joints, which hindered the possibility of evaluating the joint in a three-dimensional fashion. (7) Cartilage cortices are obliquely oriented and cannot be well evaluated on axial cuts. This is in addition to the limitations of their small sample size in that the radiologic evaluation of the joint was made on only 3 larynges.

Both of these studies failed to examine anatomic changes such as cricoarytenoid joint ankylosis, erosion, and soft-tissue changes. The results of our investigation indicate a significantly higher prevalence of ankylosis in our older group than in our younger group, as well as a trend toward joint narrowing in the older group. Our findings corroborate the results of histopathologic studies performed on the aging cricoarytenoid joint in which erosion and roughening of the joint surfaces were observed. (10,12)

Increased ankylosis and joint narrowing can also be attributable to changes affecting the synovial membrane, which constitutes the internal lining of the joint. The synovial membrane undergoes many histopathologic changes with age, including its replacement by chondrocyte clusters and a loss or decrease in its blood capillaries, macrophages, and lymphocytes. (8,12)

Our study found an asymmetry in changes affecting the cricoarytenoid joint with age. Specifically, narrowing in the aged joint was statistically significant only on the left side, which is consistent with the findings of Yeager et al, who reported an increased ossification of the cartilages and joint on the left. (6) Based on these findings, we concur that patterns of ossification affecting the cricoarytenoid joint are mainly asymmetric.

To the best of our knowledge, our study is the first to look at multiple radiologic parameters of the cricoarytenoid-joint in association with aging. Nevertheless, it does have some limitations that might be addressed in future research projects. One is its retrospective nature, which limited our ability to acquire information on our patients' phonatory behavior, voice quality, and endoscopic laryngeal findings. Another is the absence of indirect laryngeal examination, which would have been of value in excluding other possible laryngeal pathologies such as vocal fold paresis and in allowing us to draw other conclusions of possible clinical significance.

In conclusion, ankylosis and narrowing of the cricoarytenoid joint are commonly observed with aging. CT can be used to measure these changes and assist in the workup of elderly patients with dysphonia and abnormal vocal fold movement disorders.

References

(1.) Logeman JA. Upper digestive tract anatomy and physiology. In: Bailey BJ, Johnson JT, Newlands SD, eds. Head & Neck SurgeryOtolaryngology. 4th ed. Philadelphia: Lippincott Williams & Wilkins; 2006.

(2.) Sasaki C, Kim Y. Anatomy and physiology of the larynx. In: Snow JB, Ballenger J J, eds. Ballenger's Otorhinolaryngology: Head and Neck Surgery. 16th ed. Hamilton, Ont.: B.C. Decker; 2003:1090.

(3.) Sakai F, Gamsu G, Dillon WP, et al. MR imaging of the larynx at 1.5 T. J Comput Assist Tomogr 1990;14(1):60-71.

(4.) Segre R. Senescence of the voice. Eye Ear Nose Throat Mon 1971;50(6):223-7.

(5.) Huang BY, Solle M, Weissler MC. Larynx: Anatomic imaging for diagnosis and management. Otolaryngol Clin North Am 2012;45(6): 1325-61.

(6.) Yeager VL, Lawson C, Archer CR. Ossification of the laryngeal cartilages as it relates to computed tomography. Invest Radiol 1982;17(1):11-19.

(7.) Cerat J, Charlin B, Brazeau-Lamontagne L, Mongeau CJ. Assessment of the cricoarytenoid joint: High-resolution CT scan study with histo-anatomical correlation. J Otolaryngol 1988;17(2):65-7.

(8.) Meiler SM. Functional anatomy of the larynx. Otolaryngol Clin North Am 1984;17(1):3-12.

(9.) Seilars I, Seilars S. Cricoarytenoid joint structure and function. J Laryngol Otol 1983;97(ll):1027-34.

(10.) Paulsen FP, Tillmann BN. Degenerative changes in the human cricoarytenoid joint. Arch Otolaryngol Head Neck Surg 1998;124(8):903-6.

(11.) Dedivitis RA, Abrahao M, de Jesus Simoes M, et al. Cricoarytenoid joint: Histological changes during aging. Sao Paulo Med J 2001;119(2):89-90.

(12.) Kawamoto-Hirano A, Honkura Y, Shibata S, et al. Cricoarytenoid articulation in elderly Japanese with special reference to morphology of the synovial tissue. Ann Otol Rhinol Laryngol 2016;125(3):219-27.

Georges Ziade, MD; Sahar Semaan, MD; Sarah Assaad, MPH; Abdul Latif Hamdan, MD, EMBA, MPH

From the Department of Otolaryngology-Head and Neck Surgery (Dr. Ziade and Dr. Hamdan) and the Department of Radiology (Dr. Semaan), American University of Beirut Medical Center, Beirut, Lebanon; and the Department of Public Health and Primary Care, University of Cambridge, Cambridge, U.K. (Miss Assaad). The study described in this article was conducted at the American University of Beirut Medical Center.

Corresponding author: Abdul Latif Hamdan, MD, Department of Otolaryngology-Head and Neck Surgery, American University of Beirut Medical Center, PO Box 110236, Beirut, Lebanon. Email: ah77@aub.edu.lb

Caption: Figure 1. CTs demonstrate a normal-appearing cricoarytenoid joint, with preserved intra-articular soft-tissue spaces seen in each plane (arrows).

Caption: Figure 2. Joint ankylosis manifests as a loss of soft-tissue density between the cricoid and arytenoid cartilages (arrows) secondary to severe joint space narrowing, which creates areas of focal fusion.
Table 1. Distribution of sex and the four variables
by age group

                                             n (%)

                     <65 yr     [greater than or equal to] 65
Variable            (n = 49)              yr (n = 51)

Sex
 Male               27 (55.1)              25 (49.0)
 Female             22 (44.9)              26 (51.0)
Ankylosis
 Present             4 (8.2)               12 (23.5)
 Absent             45 (91.8)              39 (76.5)
Narrowing
 Present            23 (46.9)              32 (62.7)
 Absent             26 (53.1)              19(37.3)
Erosion
 Present             3(6.1)                6 (11.8)
 Absent             46 (93.9)              45 (88.2)
Increased density
 Present            20 (40.8)              23(45.1)
 Absent             29 (59.2)              28 (54.9)

Variable            p Value

Sex                  0.543
 Male
 Female
Ankylosis            0.036
 Present
 Absent
Narrowing            0.112
 Present
 Absent
Erosion              0.488
 Present
 Absent
Increased density    0.665
 Present
 Absent

Table 2. Distribution of the four variables by age and to
the side of diagnosis *

                                n (%)

                     <65 yr     [greater than or equal to] 65 yr
Variable            (n = 49)                (n = 51)

Right side
Ankylosis
 Present             3(6.1)                 11 (21.6)
 Absent             46 (93.9)               40 (78.4)
Narrowing
 Present            23 (46.9)               32 (62.7)
 Absent             26(53.1)                19(37.3)
Erosion
 Present             3(6.1)                 6 (11.8)
 Absent             46 (93.9)               45 (88.2)
Increased density
 Present            19(38.8)                18(35.3)
 Absent             30 (61.2)               33 (64.7)
Left side
Ankylosis
 Present             3(6.1)                 11 (21.6)
 Absent             46 (93.9)               40 (78.4)
Narrowing
 Present            20 (40.8)               32 (62.7)
 Absent             29 (59.2)               19(37.3)
Erosion
 Present             2(4.1)                  3 (5.9)
 Absent             47 (95.9)               48 (94.1)
Increased density
 Present            18(36.7)                21 (41.2)
 Absent             31 (63.3)               30 (58.8)

Variable            p Value

Right side
Ankylosis            0.026
 Present
 Absent
Narrowing            0.112
 Present
 Absent
Erosion              0.488
 Present
 Absent
Increased density    0.718
 Present
 Absent
Left side
Ankylosis            0.026
 Present
 Absent
Narrowing            0.028
 Present
 Absent
Erosion              1.00
 Present
 Absent
Increased density    0.649
 Present
 Absent

* Some patients exhibited bilateral involvement.

Table 3. Mean age of patients with and without the
presence/absence of the four variables

                          Age, yr, mean [+ or -] SD
Variable                       Present Absent               p Value

Ankylosis           65.5 [+ or -] 14.3 54.6 [+ or -] 18.9    0.047
Narrowing           60.2 [+ or -] 17.8 51.6 [+ or -] 18.7    0.011
Erosion             63.1 [+ or -] 23.9 55.7 [+ or -] 18.0    0.137
Increased density   57.9 [+ or -] 18.1 55.2 [+ or -] 19.0    0.497
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Article Details
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Title Annotation:ORIGINAL ARTICLE
Author:Ziade, Georges; Semaan, Sahar; Assaad, Sarah; Hamdan, Abdul Latif
Publication:Ear, Nose and Throat Journal
Article Type:Clinical report
Geographic Code:7LEBA
Date:Aug 1, 2018
Words:2852
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