- Email: [email protected]
The Cricothyroid Joint: A Practical Guide for Distinguishing Between Different Joint Types
ARTICLE IN PRESS
The Cricothyroid Joint: A Practical Guide for Distinguishing Between Different Joint Types *,1Jasmin D1X X KochD,2X X *,1D3X XFabian UntereggerD,4X X *D5X XFlurin HoneggerD6X X, †D7X XSilke PotthastD8X X, and *DClaudio 9X X StorckD10X X, *Switzerland, and
ySchlieren, Switzerland.
Abstract: Objective. Type A cricothyroid joint (CTJ) leads to a higher elongation of the vocal folds than Type B/C CTJ. Therefore, the determination for the CTJ type is important whether to perform a cricoid-thyroid approximation for a pitch elevation in transwomen with gender dysphoria. This study aimed to develop a tool for clinicians and radiologists for distinguishing between Type A (cricoid cartilage protuberance) and Type B/C (flat surface with/without cartilage of the cricoid) CTJs on high-resolution computed tomography (HRCT). Study Design. This was a prospective study. Methods. Analysis of 60 male HRCTs and 60 female HRCTs of the larynx/CTJs. Three-dimensional reconstruction of the laryngeal cartilages, based on visualization of the CTJ in HRCT scans. The intercartilaginous distances (nearest distance between the inner side of the Thyroid and outer side of the cricoid of the CTJ) were measured to compare different types of CTJs. Results. In all HRCT scans, three-dimensional reconstructions of the CTJ were feasible. All Type A CTJs showed the typical cricoid cartilage protuberance (like a volcano) in biplanar images and three-dimensional reconstructions. All Type B/C CTJs showed a flat cricoid joint cartilage in biplanar images and three-dimensional reconstructions. The type distribution was Type A: 61% in male and female larynges; Type B/C: 39% in male and female larynges. The intercartilaginous distances were Type A: 0.71 mm [0.42−0.98] in male larynges and 0.75 mm [0.44−1.40] in female larynges; Type B/C: 1.13 mm [0.36−1.24] in male larynges and 1.32 mm [0.76−2.47] in female larynges. Conclusions. In HRCT scans, the Type A CTJ showed an intercartilaginous space less than 1 mm. In contrast, the Type B/C CTJ showed an intercartilaginous distance exceeded 1 mm. Key Words: Cricoid-thyroid approximation−Cricothyroid Joint−Larynx−MIMICS−3D.
INTRODUCTION Most medical textbooks describe the larynx as a more or less static entity, consisting of three cartilages: the shieldlike thyroid, the cricoid, and the two arytenoids, which sit right above the cricoid. It has been established that the cricoid and thyroid are joined together by the cricothyroid joint (CTJ), which provides a visor-like movement, with a rotation axis running right through the joint.1 This rotation leads to an elongation of the vocal folds and to a higher voice pitch. In 1971, Maue and Dickson first described three different types of CTJs on cadaver larynges: Types A, B, and C.2 Type A has a well-defined facet. It has a tight capsule and ligaments, which form either a concavity or a small groin, directed from posterior superior to anterior inferior. The Type A joint had a typical cricoid cartilage protuberance (CCP), reminiscent of a volcanic crater, which was Accepted for publication August 29, 2018. Financial Disclosure: None. Conflict of Interest: None. Level of evidence: 4. From the *University of Basel, University Hospital, Department of Otorhinolaryngology, Head and Neck Surgery, Division of Phoniatrics, Switzerland; and the yInstitute of Radiology, Limmattal Hospital, Schlieren, aaSwitzerland. 1 Equal Co-Authors Presented at The Voice Foundations 46th Annual Symposium, June 2, 2018, Philadelphia, USA. Address correspondence and reprint requests to Claudio Storck, Department of Otorhinolaryngology, Head and Neck Surgery, Division of Phoniatrics, University Hospital Basel, Petersgraben 4, 4031 Basel, Switzerland. E-mail: [email protected] Journal of Voice, Vol. &&, No. &&, pp. 1−5 0892-1997 © 2018 The Voice Foundation. Published by Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jvoice.2018.08.019
best observed on axial high-resolution computed tomography (HRCT) images. Type B lacks a definite facet, and the two cartilaginous parts of the articulation are joined only by soft connective tissue. In contrast to Type B with its unclearly defined facet, Type C has a flat cricoid cartilage surface without a visible facet or any CCP, and the two cartilages are connected with loose soft tissues. At the time of discovery, the clinical relevance of this differentiation was not known; therefore, the CTJ hardly ever became the focus of laryngologists, phoniatricians, or radiologists. In 2010, Windisch revisited the CTJ in a cadaver study. He confirmed the three types, and provided the first description of the distributions of the different joint types in males and females. Type A was found in 56% of females and 66% of males; Type B was found in 24% of females, 20% of males; and Type C was found in 20% of females and 14% of males. Additionally, he mentioned differences in stability (vertical and horizontal sliding) among the different CTJ types.3 The technical progress made over the last decade in three-dimensional (3D) reconstruction and visualization of anatomical structures has allowed us to visualize the biomechanics of the larynx. Indeed, 3D visualizations of cadaver larynges, surgical interventions, and the larynges of professional singers have provided new insights into the biomechanics of the larynx, and particularly, the CTJ.4-7 Therefore, laryngologists and phoniatricians have turned their attention to the CTJ, because its mechanics of vocal fold elongation and stiffening have only recently been fathomed.7-9 However, we lack an exact radiological
ARTICLE IN PRESS 2 description of the articulation between the cricoid and thyroid cartilages. In previous studies, we showed that the tension and elongation of the vocal folds were significantly higher in individuals with Type A compared to those with Types B and C CTJs.7 In particular, when cricoid-thyroid-approximation (CTA) was performed to elevate the pitch in a group of transwomen with gender dysphoria, a Type A CTJ was advantageous, because it could significantly raise the vocal pitch compared to the other CTJ types.10 Keeping that in mind, it is very important that laryngologists and phoniatricians identify the patient's CTJ type preoperatively, to establish a basis for providing optimal advice to the patient. With this approach, unnecessary operations can be avoided. Previous studies were based on 3D visualizations based on MIMICS software, which is expensive, and 3D reconstructions of the CTJ, which are time-consuming. Consequently, a 3D image of the CTJ cannot be performed whenever there is a clinical question. Therefore, the present study aimed to develop criteria for laryngologists, phoniatricians, and radiologists to facilitate determinations of the CTJ type, based on HRCT images. STUDY POPULATION AND METHODS Study population This study included 60 men (mean age 57 y, range: 23−93) and 60 women (mean age 49 years, range: 30−95). Patients were excluded when the anatomical structure of the CTJ was destroyed by carcinoma. HRCT was indicated when no tumor was present in the head or neck that manifested as a vocal fold paralysis. In addition, we analyzed data from a previous approved study on professional singers. This study was approved by the Medical Ethics Committees of Zurich and Basel (Switzerland) and in all cases an informed consent was existing.
Journal of Voice, Vol. &&, No. &&, 2018
Statistical analysis For all statistical analyses, we used Matlab R2016b (V9.1.0.441655). Paired and nonpaired t tests for equal means were used. The F test was also used to compare variances and the Shapiro-Wilk test to test for normality. If a nonparametric test was indicated, we used the Wilcoxon rank sum or Wilcoxon signed rank sum test for equal medians.
RESULTS CT acquisition In all patients, we achieved diagnostic image quality, and we generated 3D images of the CTJ. Cricothyroid cartilage, thyroid cartilage, and the CTJ could be visualized nicely, with no major motion artifacts. In all larynges, the axial HRCT scans revealed the position of the CTJ. We analyzed a total of 240 CTJs (60 men and 60 women, two joints each). To identify Type A CTJs on axial HRCT scans, we looked for the typical CCP. We could not distinguish between Type B and C CTJs, because differences between these joints were not visible on axial HRCT scans and 3D reconstructed images. This finding supported our findings in earlier studies10,12 (Figure 1).
HRCT imaging All scans were performed with a clinical multislice CT scanner (Siemens Definition AS 64, Siemens Medical Solutions Erlangen, Germany), with a high-resolution technique, and with the patient in a supine position. HRCT images were sliced at a 0.8 pitch, with a 1-mm thickness, in increments of 1 mm, and a rotation time of 1 second. The voltage was set to 120 kVp, and the tube current was 150 mA. Post process imaging We postprocessed all 120 HRCT scans with Mimics software, version 14.0 (Materialise Interactive Medical Image Control System, Leuven, Belgium), as described by Storck et al.11 All CTJs were depicted as axial images. First, 3D reconstructions were performed to visualize the shape of the cricoidal part of the CTJ. Second, all axial HRCT scans were analyzed at the level of the CTJ, and the minimal intercartilaginous distance (dCT) of the CTJ was measured between the cricoid and thyroid cartilages.
FIGURE 1. 3D visualizations of the laryngeal cartilages for Type A (left column) and Types B/C (right column) cricothyroid joints (CTJs), cut at the level of the CTJs. Upper row: axial view of the cricoid cartilage: Type A shows the typical cricoid ie, cartilage protuberance (CCP), Type B/C shows a flat cartilage. Middle row: axial 3D reconstruction of the cricoid and thyroid. The intercartilaginous space between the cricoid and thyroid is narrow in Type A and wide in Types B/C. Lower row: 3D-reconstructions of the cricoid and thyroid.
ARTICLE IN PRESS Jasmin Koch, et al
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TheX XCricothyroid Joint: A Practical Guide
Distribution of the different types of CTJs Among males, we found 61% (73/120) Type A and 39% (47/ 120) Type B/C CTJs. A similar distribution was found among females: 61% (74/120) Type A and 39% (46/120) Type B/C CTJs. We then examined whether the larynges had the same (symmetric) or different (asymmetric) types of CTJs on each side. We found that, among males, 80% of larynges had symmetric CTJs (AA: 42%, CC: 38%), and 20% had asymmetric CTJs (A/BC). Among females, 78% of larynges had symmetric CTJs (AA: 45%, CC: 33%) and 22% had asymmetric CTJs.
Type A CTJs On axial HRCT images, Type A CTJs had the typical CCP at the cricoidal part of the joint (Figure 2). On 3D reconstructed images, the CCP resembled a volcanic crater. The average dCTs between thyroid and cricoid cartilages in Type A CTJs were similar in male larynges (mean: 0.71 mm, standard deviation [SD]: 0.13, 95% confidence intervals [CI] of the mean: 0.68−0.74, range: 0.42−0.98) and female larynges (mean: 0.75 mm, SD: 0.17; 95% CI of the mean: 0.71−0.78, range: 0.44−1.40; Table 1). Male and female data did not differ significantly.
Types B and C CTJs It was not possible to distinguish between Type B and Type C CTJs on axial HRCT scans or 3D reconstructed images. Therefore, we combined these two groups. The axial HRCT images showed that the cricoidal part of the joint was flat in both types (Figure 2). In 3D reconstructed images, a flat plane was also observed.
FIGURE 2. Axial views of high-resolution computed tomography scans of Type A (left) and Types B/C (right) cricothyroid joints (CTJs). Type A shows the typical cricoid cartilage protuberance (CCP), Types B/C has a flat cricoid cartilage. The boxed regions are shown at higher resolution in the lower images; the intercartilaginous distance (dCT) is depicted for both CTJ types.
TABLE 1. Mean Intercartilaginous Distances for Different Types of Cricothyroid Joints Group Male (mm) [SD, range] Female (mm), [SD, range]
Type A 0.71 [0.13, 0.42 −0.98] 0.75 [0.17, 0.44 −1.40]
Type B/C 1.13 [0.36, 1.03 −1.24] 1.32 [0.45, 0.76 −2.47]
SD, standard deviation.
The average dCT between the thyroid and cricoid cartilages was similar in male larynges (mean: 1.13 mm, SD: 0.36, 95% CI of the mean: 1.03−1.24) and female larynges (mean: 1.32 mm, SD: 0.45; 95% CI of the mean: 1.20−1.46, range 0.76−2.47; Table 1). Male and female data did not differ significantly. Intercartilaginous distance as a predictor of the CTJ type Figure 3 demonstrates the difference between dCTs in Type A and Type B/C CTJs. For this analysis, we pooled the data for males and females because, as stated in the previous sections, we found no significant differences between the sexes. Type A CTJs had a mean dCT of 0.73 mm (SD: 0.14, 95% CI of the mean: 0.70−0.75 mm, range: 0.42−1.40). Type B/C CTJs had a mean dCT of 1.32 mm (SD: 0.42, 95% CI of the mean: 0.56−2.47, range: 0.56−2.47). The two means differed significantly (t test, P < 10¡29). Moreover, we investigated how the dCT values of these two groups overlapped to determine a means to distinguish between the groups. We superimposed the Gaussian probability densities of the dCTs, weighted by their prior probabilities of 61% and 39% for Type A and Type B/C CTJs (Figure 3). At a distance of 1.0034 mm (dotted line, Figure 3), there was a 50% a posteriori probability that the CTJ could be either a Type A or Type B/C (ie, this is where the probability densities intersect). Lower dCTs indicated a higher probability that the CTJ was Type A, rather than Type B/C. At a distance of 0.9457 mm (dashed line, Figure 3), the probability that the CTJ corresponded to a Type A was twice as high as its probability of corresponding to a Type B/C (66.6% vs 33.3%). DISCUSSION Most macroscopic human anatomy has been explored and examined. In particular, the joints and their ranges of motion have been examined with both biomechanical and imaging techniques, primarily with regard to orthopedic surgery. However, only a few authors have examined the laryngeal joints.13-15 It was not until 1971 that Maue and Dickson examined the CTJ anatomically. They found anatomic variations2 that distinguished three types of CTJs. The Type A CTJ has a CCP with a well-defined cartilaginous facet, and a tight capsule. The Type B CTJ had a flat
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FIGURE 3. Intercartilaginous distances for Types A and B/C. The mean intercartilaginous distances are 0.73 mm for Type A and 1.32 mm for Types B/C. The two means differ significantly (t test, P < 10¡29). cricoid, a cartilaginous facet, and soft connective tissues that connect the two cartilaginous parts. The Type C CTJ had a flat cricoid with no cartilaginous facet, but with soft connective tissue. Ultimately, the accepted view was that the virtual rotation axis of the cricoid runs through the two CTJs. Anatomically and functionally the cricothyroid muscles originate on the cricoid and insert on the thyroid, so in essence they are pulling the thyroid cartilage forward and downward toward the cricoid, like “closing a visor” on a helmet. In other words, the cricoid rotates (or the thyroid rotates) around this axis running through both CTJs, when the cricothyroid muscles contract. Hammer and Windisch confirmed this observation in the early 2000s.3,4 It was not until the introduction of high-resolution imaging techniques and later, 3D visualization, that it became possible to examine this particular joint closely. Storck et al first showed, on a 3D reconstructed cadaver larynx, that the virtual rotational axis depended on the CJT Type. In a Type A CTJ, the rotational axis ran through or near the CTJs. In a Type B CTJ, the axis ran above the CTJ. In a Type C CTJ, the rotational axis ran through the top of the cricoid, away from the CTJ.7 Those distinct findings could be explained by the different anatomies of the joint capsules, as described by Maue and Dickson.2 The tight capsules of the Type A CTJ do not allow much shifting during CTJ movements, as Hammer described previously.4 Therefore, there is a rotational movement about an axis that goes through (or near) the CTJ. In Type C CTJs, there is a loose joint capsule, which allows large shifts of the inferior thyroid process during CT muscle activation.4 In cadaver studies, Storck et al showed that the joint type influenced the location of the rotational axis, and thus, the elongation of the vocal folds.7 They also
Journal of Voice, Vol. &&, No. &&, 2018
showed that this feature could be exploited in CTA, a procedure for increasing the voice pitch in transwomen with gender dysphoria.10 Actually the CTA (Type IV Isshiki thyroplasty) specifically approximates the anterior and anterolateral thyroid and cricoid cartilages (everything anterior to the CT joints), and usually bilaterally, although it can be a unilateral operation. This intervention causes an elongation in the vocal fold. Due to significantly better results, it was postulated that CTA surgery should only be planned for patients with Type A CTJs.10 Thus, in future, there might be more requests to determine patient joint types, from laryngologists to radiologists. When a patient does not have a Type A CTJ, the laryngologist should consider another surgical method, eg, a glottoplasty or a feminization larygoplasty.16 To undergird this statement, we need a study analyzing only CTA in Type A CTJs patients over a long term. 3D rendering of the laryngeal cartilages is time consuming and the software is expensive for everyday use in clinical practice. Therefore, there is a need for criteria that radiologists can use to distinguish between the different CTJ types in axial HRCTs to rule out Types B/C for a CTA quickly. Here, based on 240 axial HRCT images, we showed that a Type A CTJ can clearly be differentiated from a Type B/C joint. The Type A joint had a typical CCP, reminiscent of a volcanic crater, which was best observed on axial images. We could not distinguish between Type B and C CTJs in biplanar images, but in fact, this distinction was not clinically relevant. On the other hand, the dCT was of interest. Type A CTJs had significantly smaller dCTs (<1 mm) than Type B/C CTJs (>1 mm). We showed that the probability of identifying a Type A CTJ increased when the dCT was less than 1.0034 mm. CONCLUSIONS In this study, we provided a tool for radiologists that will be useful for identifying the different types of CTJs, based on morphology and the dCT. These findings can be communicated to laryngologists. The CTJ can be clearly identified in an ordinary neck CT, when the reader is aware of the distinguishing features. The proper facet and joint capsule renders Type A readily detectable on the HRCT. Types B and C CTJs are both formed with soft tissue components; therefore, they are not readily distinguishable, compared to Type A. The outcome of CTA surgery depends on the type of CTJ.10 Thus, it is important for radiologists to become more familiar with this fairly unfamiliar joint. Therefore, we recommend the following procedure. First, the CTJ should be identified on axial HRCT scans (Figure 2). A CCP is typical for Type A CTJs. A flat rounded cricoid could be a Type B or C CTJ. Second, the dCT of the CTJ should be measured on axial HRCT scans (Figure 2). For distances shorter than 1 mm, there is a favorable probability that the CTJ is Type A, and the
ARTICLE IN PRESS Jasmin Koch, et al
TheX XCricothyroid Joint: A Practical Guide
probability increases as the distance decreases. For distances greater than 1 mm, there is a high probability that the CTJ is Type B/C. Acknowledgments This study was financially supported by the GoldschmidtJacobson Foundation and the Gottfried Bangerter−Rhyner Foundation. REFERENCES 1. Rosen CASB. Anatomy and Physiology of the Larynx. Operative Techniques in Laryngology. Chapter I:. Berlin, Heidelberg: Springer; 2008. 2. Maue WM, Dickson DR. Cartilages and ligaments of the adult human larynx. Arch Otolaryngol. 1971;94:432–439. 3. Windisch G, Hammer G, Prodinger P, et al. The functional anatomy of the cricothyroid joint. Surg Radiologic Anat. 2010;32:135–139. 4. Hammer G, Windisch G, Prodinger P, et al. The cricothyroid joint −functional aspects with regard to different types of its structure. J Voice. 2010;24:140–145. 5. Storck C, Gugatschka M, Friedrich G, et al. Developing a 3D model of the laryngeal cartilages using HRCT data and MIMICS's segmentation software. Logopedics Phoniatrics, Vocol. 2010;35:19–23. 6. Storck C, Juergens P, Fischer C, et al. Three-dimensional imaging of the larynx for pre-operative planning of laryngeal framework surgery. Eur Arch Oto-Rhino-Laryngol. 2010;267:557–563.
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7. Storck C, Gehrer R, Fischer C, et al. The role of the cricothyroid joint anatomy in cricothyroid approximation surgery. J Voice. 2011;25:632– 637. 8. Unteregger F, Honegger F, Potthast S, et al. 3D analysis of the movements of the laryngeal cartilages during singing. Laryngoscope. 2017;127:1639–1643. 9. Storck C, Unteregger F. Cricothyroid joint type as predictor for vocal fold elongation in professional singers. Laryngoscope 2017. http://dx.doi.org/10.1002/lary.26984. Nov 8 [Epub ahead of print]. 10. Tschan S, Honegger F, Storck C. Cricothyroid joint anatomy as a predicting factor for success of cricoid-thyroid approximation in transwomen. Laryngoscope. 2016;126:1380–1384. 11. Storck C, Gugatschka M, Friedrich G, et al. Developing a 3D model of the laryngeal cartilages using HRCT data and MIMICS's segmentation software. Logoped Phoniatr Vocol. 2010;35:19–23. 12. Vorik A, Unteregger F, Zwicky S, et al. Three-dimensional imaging of high-resolution computer tomography of Singers' Larynges-A pilot study. J Voice. 2017;31:115. e117-115 e121. 13. von L, Moore P. The mechanics of the cricoarytenoid joint. Arch Otolaryngol. 1961;73:541–550. 14. Frable MA. Computation of motion at the cricoarytenoid joint. Arch Otolaryngol. 1961;73:551–556. 15. Sellars IE, Keen EN. The anatomy and movements of the cricoarytenoid joint. Laryngoscope. 1978;88:667–674. 16. Mora E, Cobeta I, Becerra A, et al. Comparison of cricothyroid approximation and glottoplasty for surgical voice feminization in male-to-female transsexuals. Laryngoscope 2017.
The Cricothyroid Joint: A Practical Guide for Distinguishing Between Different Joint Types *,1Jasmin D1X X KochD,2X X *,1D3X XFabian UntereggerD,4X X *D5X XFlurin HoneggerD6X X, †D7X XSilke PotthastD8X X, and *DClaudio 9X X StorckD10X X, *Switzerland, and
ySchlieren, Switzerland.
Abstract: Objective. Type A cricothyroid joint (CTJ) leads to a higher elongation of the vocal folds than Type B/C CTJ. Therefore, the determination for the CTJ type is important whether to perform a cricoid-thyroid approximation for a pitch elevation in transwomen with gender dysphoria. This study aimed to develop a tool for clinicians and radiologists for distinguishing between Type A (cricoid cartilage protuberance) and Type B/C (flat surface with/without cartilage of the cricoid) CTJs on high-resolution computed tomography (HRCT). Study Design. This was a prospective study. Methods. Analysis of 60 male HRCTs and 60 female HRCTs of the larynx/CTJs. Three-dimensional reconstruction of the laryngeal cartilages, based on visualization of the CTJ in HRCT scans. The intercartilaginous distances (nearest distance between the inner side of the Thyroid and outer side of the cricoid of the CTJ) were measured to compare different types of CTJs. Results. In all HRCT scans, three-dimensional reconstructions of the CTJ were feasible. All Type A CTJs showed the typical cricoid cartilage protuberance (like a volcano) in biplanar images and three-dimensional reconstructions. All Type B/C CTJs showed a flat cricoid joint cartilage in biplanar images and three-dimensional reconstructions. The type distribution was Type A: 61% in male and female larynges; Type B/C: 39% in male and female larynges. The intercartilaginous distances were Type A: 0.71 mm [0.42−0.98] in male larynges and 0.75 mm [0.44−1.40] in female larynges; Type B/C: 1.13 mm [0.36−1.24] in male larynges and 1.32 mm [0.76−2.47] in female larynges. Conclusions. In HRCT scans, the Type A CTJ showed an intercartilaginous space less than 1 mm. In contrast, the Type B/C CTJ showed an intercartilaginous distance exceeded 1 mm. Key Words: Cricoid-thyroid approximation−Cricothyroid Joint−Larynx−MIMICS−3D.
INTRODUCTION Most medical textbooks describe the larynx as a more or less static entity, consisting of three cartilages: the shieldlike thyroid, the cricoid, and the two arytenoids, which sit right above the cricoid. It has been established that the cricoid and thyroid are joined together by the cricothyroid joint (CTJ), which provides a visor-like movement, with a rotation axis running right through the joint.1 This rotation leads to an elongation of the vocal folds and to a higher voice pitch. In 1971, Maue and Dickson first described three different types of CTJs on cadaver larynges: Types A, B, and C.2 Type A has a well-defined facet. It has a tight capsule and ligaments, which form either a concavity or a small groin, directed from posterior superior to anterior inferior. The Type A joint had a typical cricoid cartilage protuberance (CCP), reminiscent of a volcanic crater, which was Accepted for publication August 29, 2018. Financial Disclosure: None. Conflict of Interest: None. Level of evidence: 4. From the *University of Basel, University Hospital, Department of Otorhinolaryngology, Head and Neck Surgery, Division of Phoniatrics, Switzerland; and the yInstitute of Radiology, Limmattal Hospital, Schlieren, aaSwitzerland. 1 Equal Co-Authors Presented at The Voice Foundations 46th Annual Symposium, June 2, 2018, Philadelphia, USA. Address correspondence and reprint requests to Claudio Storck, Department of Otorhinolaryngology, Head and Neck Surgery, Division of Phoniatrics, University Hospital Basel, Petersgraben 4, 4031 Basel, Switzerland. E-mail: [email protected] Journal of Voice, Vol. &&, No. &&, pp. 1−5 0892-1997 © 2018 The Voice Foundation. Published by Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jvoice.2018.08.019
best observed on axial high-resolution computed tomography (HRCT) images. Type B lacks a definite facet, and the two cartilaginous parts of the articulation are joined only by soft connective tissue. In contrast to Type B with its unclearly defined facet, Type C has a flat cricoid cartilage surface without a visible facet or any CCP, and the two cartilages are connected with loose soft tissues. At the time of discovery, the clinical relevance of this differentiation was not known; therefore, the CTJ hardly ever became the focus of laryngologists, phoniatricians, or radiologists. In 2010, Windisch revisited the CTJ in a cadaver study. He confirmed the three types, and provided the first description of the distributions of the different joint types in males and females. Type A was found in 56% of females and 66% of males; Type B was found in 24% of females, 20% of males; and Type C was found in 20% of females and 14% of males. Additionally, he mentioned differences in stability (vertical and horizontal sliding) among the different CTJ types.3 The technical progress made over the last decade in three-dimensional (3D) reconstruction and visualization of anatomical structures has allowed us to visualize the biomechanics of the larynx. Indeed, 3D visualizations of cadaver larynges, surgical interventions, and the larynges of professional singers have provided new insights into the biomechanics of the larynx, and particularly, the CTJ.4-7 Therefore, laryngologists and phoniatricians have turned their attention to the CTJ, because its mechanics of vocal fold elongation and stiffening have only recently been fathomed.7-9 However, we lack an exact radiological
ARTICLE IN PRESS 2 description of the articulation between the cricoid and thyroid cartilages. In previous studies, we showed that the tension and elongation of the vocal folds were significantly higher in individuals with Type A compared to those with Types B and C CTJs.7 In particular, when cricoid-thyroid-approximation (CTA) was performed to elevate the pitch in a group of transwomen with gender dysphoria, a Type A CTJ was advantageous, because it could significantly raise the vocal pitch compared to the other CTJ types.10 Keeping that in mind, it is very important that laryngologists and phoniatricians identify the patient's CTJ type preoperatively, to establish a basis for providing optimal advice to the patient. With this approach, unnecessary operations can be avoided. Previous studies were based on 3D visualizations based on MIMICS software, which is expensive, and 3D reconstructions of the CTJ, which are time-consuming. Consequently, a 3D image of the CTJ cannot be performed whenever there is a clinical question. Therefore, the present study aimed to develop criteria for laryngologists, phoniatricians, and radiologists to facilitate determinations of the CTJ type, based on HRCT images. STUDY POPULATION AND METHODS Study population This study included 60 men (mean age 57 y, range: 23−93) and 60 women (mean age 49 years, range: 30−95). Patients were excluded when the anatomical structure of the CTJ was destroyed by carcinoma. HRCT was indicated when no tumor was present in the head or neck that manifested as a vocal fold paralysis. In addition, we analyzed data from a previous approved study on professional singers. This study was approved by the Medical Ethics Committees of Zurich and Basel (Switzerland) and in all cases an informed consent was existing.
Journal of Voice, Vol. &&, No. &&, 2018
Statistical analysis For all statistical analyses, we used Matlab R2016b (V9.1.0.441655). Paired and nonpaired t tests for equal means were used. The F test was also used to compare variances and the Shapiro-Wilk test to test for normality. If a nonparametric test was indicated, we used the Wilcoxon rank sum or Wilcoxon signed rank sum test for equal medians.
RESULTS CT acquisition In all patients, we achieved diagnostic image quality, and we generated 3D images of the CTJ. Cricothyroid cartilage, thyroid cartilage, and the CTJ could be visualized nicely, with no major motion artifacts. In all larynges, the axial HRCT scans revealed the position of the CTJ. We analyzed a total of 240 CTJs (60 men and 60 women, two joints each). To identify Type A CTJs on axial HRCT scans, we looked for the typical CCP. We could not distinguish between Type B and C CTJs, because differences between these joints were not visible on axial HRCT scans and 3D reconstructed images. This finding supported our findings in earlier studies10,12 (Figure 1).
HRCT imaging All scans were performed with a clinical multislice CT scanner (Siemens Definition AS 64, Siemens Medical Solutions Erlangen, Germany), with a high-resolution technique, and with the patient in a supine position. HRCT images were sliced at a 0.8 pitch, with a 1-mm thickness, in increments of 1 mm, and a rotation time of 1 second. The voltage was set to 120 kVp, and the tube current was 150 mA. Post process imaging We postprocessed all 120 HRCT scans with Mimics software, version 14.0 (Materialise Interactive Medical Image Control System, Leuven, Belgium), as described by Storck et al.11 All CTJs were depicted as axial images. First, 3D reconstructions were performed to visualize the shape of the cricoidal part of the CTJ. Second, all axial HRCT scans were analyzed at the level of the CTJ, and the minimal intercartilaginous distance (dCT) of the CTJ was measured between the cricoid and thyroid cartilages.
FIGURE 1. 3D visualizations of the laryngeal cartilages for Type A (left column) and Types B/C (right column) cricothyroid joints (CTJs), cut at the level of the CTJs. Upper row: axial view of the cricoid cartilage: Type A shows the typical cricoid ie, cartilage protuberance (CCP), Type B/C shows a flat cartilage. Middle row: axial 3D reconstruction of the cricoid and thyroid. The intercartilaginous space between the cricoid and thyroid is narrow in Type A and wide in Types B/C. Lower row: 3D-reconstructions of the cricoid and thyroid.
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Distribution of the different types of CTJs Among males, we found 61% (73/120) Type A and 39% (47/ 120) Type B/C CTJs. A similar distribution was found among females: 61% (74/120) Type A and 39% (46/120) Type B/C CTJs. We then examined whether the larynges had the same (symmetric) or different (asymmetric) types of CTJs on each side. We found that, among males, 80% of larynges had symmetric CTJs (AA: 42%, CC: 38%), and 20% had asymmetric CTJs (A/BC). Among females, 78% of larynges had symmetric CTJs (AA: 45%, CC: 33%) and 22% had asymmetric CTJs.
Type A CTJs On axial HRCT images, Type A CTJs had the typical CCP at the cricoidal part of the joint (Figure 2). On 3D reconstructed images, the CCP resembled a volcanic crater. The average dCTs between thyroid and cricoid cartilages in Type A CTJs were similar in male larynges (mean: 0.71 mm, standard deviation [SD]: 0.13, 95% confidence intervals [CI] of the mean: 0.68−0.74, range: 0.42−0.98) and female larynges (mean: 0.75 mm, SD: 0.17; 95% CI of the mean: 0.71−0.78, range: 0.44−1.40; Table 1). Male and female data did not differ significantly.
Types B and C CTJs It was not possible to distinguish between Type B and Type C CTJs on axial HRCT scans or 3D reconstructed images. Therefore, we combined these two groups. The axial HRCT images showed that the cricoidal part of the joint was flat in both types (Figure 2). In 3D reconstructed images, a flat plane was also observed.
FIGURE 2. Axial views of high-resolution computed tomography scans of Type A (left) and Types B/C (right) cricothyroid joints (CTJs). Type A shows the typical cricoid cartilage protuberance (CCP), Types B/C has a flat cricoid cartilage. The boxed regions are shown at higher resolution in the lower images; the intercartilaginous distance (dCT) is depicted for both CTJ types.
TABLE 1. Mean Intercartilaginous Distances for Different Types of Cricothyroid Joints Group Male (mm) [SD, range] Female (mm), [SD, range]
Type A 0.71 [0.13, 0.42 −0.98] 0.75 [0.17, 0.44 −1.40]
Type B/C 1.13 [0.36, 1.03 −1.24] 1.32 [0.45, 0.76 −2.47]
SD, standard deviation.
The average dCT between the thyroid and cricoid cartilages was similar in male larynges (mean: 1.13 mm, SD: 0.36, 95% CI of the mean: 1.03−1.24) and female larynges (mean: 1.32 mm, SD: 0.45; 95% CI of the mean: 1.20−1.46, range 0.76−2.47; Table 1). Male and female data did not differ significantly. Intercartilaginous distance as a predictor of the CTJ type Figure 3 demonstrates the difference between dCTs in Type A and Type B/C CTJs. For this analysis, we pooled the data for males and females because, as stated in the previous sections, we found no significant differences between the sexes. Type A CTJs had a mean dCT of 0.73 mm (SD: 0.14, 95% CI of the mean: 0.70−0.75 mm, range: 0.42−1.40). Type B/C CTJs had a mean dCT of 1.32 mm (SD: 0.42, 95% CI of the mean: 0.56−2.47, range: 0.56−2.47). The two means differed significantly (t test, P < 10¡29). Moreover, we investigated how the dCT values of these two groups overlapped to determine a means to distinguish between the groups. We superimposed the Gaussian probability densities of the dCTs, weighted by their prior probabilities of 61% and 39% for Type A and Type B/C CTJs (Figure 3). At a distance of 1.0034 mm (dotted line, Figure 3), there was a 50% a posteriori probability that the CTJ could be either a Type A or Type B/C (ie, this is where the probability densities intersect). Lower dCTs indicated a higher probability that the CTJ was Type A, rather than Type B/C. At a distance of 0.9457 mm (dashed line, Figure 3), the probability that the CTJ corresponded to a Type A was twice as high as its probability of corresponding to a Type B/C (66.6% vs 33.3%). DISCUSSION Most macroscopic human anatomy has been explored and examined. In particular, the joints and their ranges of motion have been examined with both biomechanical and imaging techniques, primarily with regard to orthopedic surgery. However, only a few authors have examined the laryngeal joints.13-15 It was not until 1971 that Maue and Dickson examined the CTJ anatomically. They found anatomic variations2 that distinguished three types of CTJs. The Type A CTJ has a CCP with a well-defined cartilaginous facet, and a tight capsule. The Type B CTJ had a flat
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FIGURE 3. Intercartilaginous distances for Types A and B/C. The mean intercartilaginous distances are 0.73 mm for Type A and 1.32 mm for Types B/C. The two means differ significantly (t test, P < 10¡29). cricoid, a cartilaginous facet, and soft connective tissues that connect the two cartilaginous parts. The Type C CTJ had a flat cricoid with no cartilaginous facet, but with soft connective tissue. Ultimately, the accepted view was that the virtual rotation axis of the cricoid runs through the two CTJs. Anatomically and functionally the cricothyroid muscles originate on the cricoid and insert on the thyroid, so in essence they are pulling the thyroid cartilage forward and downward toward the cricoid, like “closing a visor” on a helmet. In other words, the cricoid rotates (or the thyroid rotates) around this axis running through both CTJs, when the cricothyroid muscles contract. Hammer and Windisch confirmed this observation in the early 2000s.3,4 It was not until the introduction of high-resolution imaging techniques and later, 3D visualization, that it became possible to examine this particular joint closely. Storck et al first showed, on a 3D reconstructed cadaver larynx, that the virtual rotational axis depended on the CJT Type. In a Type A CTJ, the rotational axis ran through or near the CTJs. In a Type B CTJ, the axis ran above the CTJ. In a Type C CTJ, the rotational axis ran through the top of the cricoid, away from the CTJ.7 Those distinct findings could be explained by the different anatomies of the joint capsules, as described by Maue and Dickson.2 The tight capsules of the Type A CTJ do not allow much shifting during CTJ movements, as Hammer described previously.4 Therefore, there is a rotational movement about an axis that goes through (or near) the CTJ. In Type C CTJs, there is a loose joint capsule, which allows large shifts of the inferior thyroid process during CT muscle activation.4 In cadaver studies, Storck et al showed that the joint type influenced the location of the rotational axis, and thus, the elongation of the vocal folds.7 They also
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showed that this feature could be exploited in CTA, a procedure for increasing the voice pitch in transwomen with gender dysphoria.10 Actually the CTA (Type IV Isshiki thyroplasty) specifically approximates the anterior and anterolateral thyroid and cricoid cartilages (everything anterior to the CT joints), and usually bilaterally, although it can be a unilateral operation. This intervention causes an elongation in the vocal fold. Due to significantly better results, it was postulated that CTA surgery should only be planned for patients with Type A CTJs.10 Thus, in future, there might be more requests to determine patient joint types, from laryngologists to radiologists. When a patient does not have a Type A CTJ, the laryngologist should consider another surgical method, eg, a glottoplasty or a feminization larygoplasty.16 To undergird this statement, we need a study analyzing only CTA in Type A CTJs patients over a long term. 3D rendering of the laryngeal cartilages is time consuming and the software is expensive for everyday use in clinical practice. Therefore, there is a need for criteria that radiologists can use to distinguish between the different CTJ types in axial HRCTs to rule out Types B/C for a CTA quickly. Here, based on 240 axial HRCT images, we showed that a Type A CTJ can clearly be differentiated from a Type B/C joint. The Type A joint had a typical CCP, reminiscent of a volcanic crater, which was best observed on axial images. We could not distinguish between Type B and C CTJs in biplanar images, but in fact, this distinction was not clinically relevant. On the other hand, the dCT was of interest. Type A CTJs had significantly smaller dCTs (<1 mm) than Type B/C CTJs (>1 mm). We showed that the probability of identifying a Type A CTJ increased when the dCT was less than 1.0034 mm. CONCLUSIONS In this study, we provided a tool for radiologists that will be useful for identifying the different types of CTJs, based on morphology and the dCT. These findings can be communicated to laryngologists. The CTJ can be clearly identified in an ordinary neck CT, when the reader is aware of the distinguishing features. The proper facet and joint capsule renders Type A readily detectable on the HRCT. Types B and C CTJs are both formed with soft tissue components; therefore, they are not readily distinguishable, compared to Type A. The outcome of CTA surgery depends on the type of CTJ.10 Thus, it is important for radiologists to become more familiar with this fairly unfamiliar joint. Therefore, we recommend the following procedure. First, the CTJ should be identified on axial HRCT scans (Figure 2). A CCP is typical for Type A CTJs. A flat rounded cricoid could be a Type B or C CTJ. Second, the dCT of the CTJ should be measured on axial HRCT scans (Figure 2). For distances shorter than 1 mm, there is a favorable probability that the CTJ is Type A, and the
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probability increases as the distance decreases. For distances greater than 1 mm, there is a high probability that the CTJ is Type B/C. Acknowledgments This study was financially supported by the GoldschmidtJacobson Foundation and the Gottfried Bangerter−Rhyner Foundation. REFERENCES 1. Rosen CASB. Anatomy and Physiology of the Larynx. Operative Techniques in Laryngology. Chapter I:. Berlin, Heidelberg: Springer; 2008. 2. Maue WM, Dickson DR. Cartilages and ligaments of the adult human larynx. Arch Otolaryngol. 1971;94:432–439. 3. Windisch G, Hammer G, Prodinger P, et al. The functional anatomy of the cricothyroid joint. Surg Radiologic Anat. 2010;32:135–139. 4. Hammer G, Windisch G, Prodinger P, et al. The cricothyroid joint −functional aspects with regard to different types of its structure. J Voice. 2010;24:140–145. 5. Storck C, Gugatschka M, Friedrich G, et al. Developing a 3D model of the laryngeal cartilages using HRCT data and MIMICS's segmentation software. Logopedics Phoniatrics, Vocol. 2010;35:19–23. 6. Storck C, Juergens P, Fischer C, et al. Three-dimensional imaging of the larynx for pre-operative planning of laryngeal framework surgery. Eur Arch Oto-Rhino-Laryngol. 2010;267:557–563.
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7. Storck C, Gehrer R, Fischer C, et al. The role of the cricothyroid joint anatomy in cricothyroid approximation surgery. J Voice. 2011;25:632– 637. 8. Unteregger F, Honegger F, Potthast S, et al. 3D analysis of the movements of the laryngeal cartilages during singing. Laryngoscope. 2017;127:1639–1643. 9. Storck C, Unteregger F. Cricothyroid joint type as predictor for vocal fold elongation in professional singers. Laryngoscope 2017. http://dx.doi.org/10.1002/lary.26984. Nov 8 [Epub ahead of print]. 10. Tschan S, Honegger F, Storck C. Cricothyroid joint anatomy as a predicting factor for success of cricoid-thyroid approximation in transwomen. Laryngoscope. 2016;126:1380–1384. 11. Storck C, Gugatschka M, Friedrich G, et al. Developing a 3D model of the laryngeal cartilages using HRCT data and MIMICS's segmentation software. Logoped Phoniatr Vocol. 2010;35:19–23. 12. Vorik A, Unteregger F, Zwicky S, et al. Three-dimensional imaging of high-resolution computer tomography of Singers' Larynges-A pilot study. J Voice. 2017;31:115. e117-115 e121. 13. von L, Moore P. The mechanics of the cricoarytenoid joint. Arch Otolaryngol. 1961;73:541–550. 14. Frable MA. Computation of motion at the cricoarytenoid joint. Arch Otolaryngol. 1961;73:551–556. 15. Sellars IE, Keen EN. The anatomy and movements of the cricoarytenoid joint. Laryngoscope. 1978;88:667–674. 16. Mora E, Cobeta I, Becerra A, et al. Comparison of cricothyroid approximation and glottoplasty for surgical voice feminization in male-to-female transsexuals. Laryngoscope 2017.