A Morphometric Study of the Semicircular Canals Using Micro-CT Images in Three-Dimensional Reconstruction

Authors


Correspondence to: Ki-Seok Koh, Department of Anatomy, Research Institute of Medical Science, Konkuk University School of Medicine, 1 Hwayang-dong, Gwangjin-gu, Seoul 143-701, Republic of Korea. Fax: +82-2-20307845. E-mail: kskoh@kku.ac.kr

Abstract

It is generally accepted that the three semicircular canals are set at right angles to each other and the lateral semicircular canal is smaller than the anterior and posterior semicircular canals. Precise knowledge of the size and spatial relationships of the semicircular canals is vital, and so the 40 petrous parts of the temporal bones were scanned by micro-CT at a slice thickness of 35 µm. The micro-CT images were used in reconstructing three-dimensional models of the bony labyrinth using computer software. Various dimensions of the semicircular canals were measured using the software, and statistical analysis was performed. The anterior semicircular canal was slightly wider than the posterior semicircular canal, and their heights were similar. The radius of curvature of the lateral semicircular canal was 20% smaller than those of the anterior and posterior semicircular canals. The angles between the three canals were not exactly 90 degrees: they were 92.1, 84.4, and 86.2 degrees between the anterior and posterior, anterior and lateral, and posterior and lateral semicircular canals, respectively. We obtained high-resolution images of the semicircular canals using three-dimensional reconstruction software, and these were used to precisely measure the angles between the semicircular canals and the area of the distorted circle formed by each semicircular canal. Anat Rec, 296:834–839, 2013. © 2013 Wiley Periodicals, Inc.

The bony labyrinth in the petrous part of the temporal bone contains the organs of hearing and balance. The vestibule and semicircular canals (SCCs) are involved in the registration of head movements (Spoor and Zonneveld, 1998). Because the SCCs are confined to the bony otic capsule, the hardest and most compact bone in the skeleton, they are difficult to dissect. This makes it difficult to observe the entire gross anatomy of the SCCs. Most previous anatomical studies of the SCCs have used conventional computed tomography (CT) (Spoor and Zonneveld, 1995, 1998; Spoor et al., 2003; Welker et al., 2009; Yamashita et al., 2011; Yuan et al., 2012), and a few studies were focused on the morphology of the SCCs themselves. Spoor and Zonneveld (1995) measured the size of the SCCs using CT images and reported the outward appearance of the bony labyrinth among diverse primates using CT images of dry skulls (Spoor and Zonneveld, 1998). Although that study provided high-resolution images, CT images of the SCCs are inadequate for revealing the detailed morphology. The conventional CT images of the SCCs were suitable for clinical diagnosis or assessment. However, it was not appropriate for investigation of whole morphology of SCCs because of the sizes of SCCs were too small. Moreover, accurate measurements of the SCCs are difficult in a two-dimensional (2D) plane because they are performed on the same transverse and sagittal planes in CT images. In addition, the true dimension is a 3D parameter, which is not necessarily presented in the selected image plane. The limitations of 2D approaches can be overcome using computer-assisted three-dimensional (3D) reconstruction (Bloch and Sørensen, 2010).

In the present study, the SCCs were reconstructed in three dimensions after scanning with high-resolution micro-CT. In addition, a high-resolution 3D model of the SCCs was reconstructed using computer software. Finally, we obtained actual data on dimensions of the SCCs and the angles between them.

MATERIALS AND METHODS

Forty petrous parts of the temporal bones were obtained from 23 donated cadavers fixed with formalin (12 males, 11 females; mean age 65.6 years, range 23–96 years). The use of body tissue for research or education was allowed by donor or donor's family. The specimens were wrapped to prevent drying. Serial micro-CT images of the specimens were acquired in the sagittal plane at a slice thickness of 35 µm (model 1076, Skyscan, Kontich, Belgium). The images were converted into JPEG files to facilitate image processing. Micro-CT images that included the cochlea, SCCs, vestibule, round window, and oval window were selected. The selected images were cropped in Adobe Photoshop CS4 (Adobe Systems, San Jose, USA) so that they included only the bony labyrinth. Because the original image of the temporal bone was too large to reconstruct, the images had to be cropped including whole inner ear structures. The cropped images were used in reconstructing 3D images of the bony labyrinth using Lucion software (Cybermed, Seoul, Korea). The 3D reconstruction of the inner ear structure was made automatically in the program, therefore there was no manual segmentation by authors. Based on the 3D model, nine dimensions of the SCC were measured using the software. The 3D models of the SCCs were aligned with parallel plane in front of view showing the largest diameter of each SCC before measurement. The various dimensions of the SCCs were measured using a 3D ruler in the program since the results for the 2D ruler varied with the angle. The measurement value using 3D ruler tool of the program is constant regardless of the view or angle if the landmark is accurate and constant.

The anterior SCC, posterior SCC, and lateral SCC are henceforth referred to as the ASCC, PSCC, and LSCC, respectively. The following dimensions were measured (Fig. 1):

  1. Widths of the three SCCs.
  2. Heights of the three SCCs.
  3. Internal widths of the three SCCs.
  4. Internal heights of the three SCCs.
  5. Areas of the distorted circles of the three SCCs.
  6. Perimeters of the distorted circles of the three SCCs.
  7. Angles between the ASCC, PSCC, and LSCC.
  8. Length of the common crus.
  9. Width of the common crus.
Figure 1.

Landmarks and measurements of the SCCs. A: Heights and widths of the SCCs (ASCC, PSCC, and LSCC are shown from left to right). B: Internal widths and internal heights of the SCCs, and areas and perimeters of their distorted circles. Internal widths and internal heights of the SCCs were measured perpendicularly at three points from the distal common crus to the proximal common crus. Thinner arrows indicate the internal heights of the SCCs. C: Angles between the ASCC and PSCC, ASCC and LSCC, and PSCC and LSCC (from left to right). D: Length and width of the common crus. The width was measured at three points.

Internal widths and heights of the three SCCs were measured perpendicularly. The ASCC and PSCC share a common crus that is located between them. Independent t test between males and females, and paired t tests between the left and right sides were performed using SPSS Statistics (ver. 19, SPSS, New York).

RESULTS

The only measured dimensions of the bony labyrinth that differed between males and females were the areas and perimeters of the PSCC circle (P<0.05), and none of the dimensions differed between the left and right sides (P>0.05). Thus the data for both genders are presented in the tables. The ASCC and PSCC had similar heights and widths (P>0.05), but the LSCC was smaller than the other two SCCs (P<0.05). To confirm the measurements, the radius of curvature of each canal arc was calculated by taking half the average of the height and width measurements [0.5(height+width)/2], in accordance with a previous study (Spoor and Zonneveld, 1998). The radii of curvature of the ASCC and PSCC were similar, but that of the LSCC was 20% smaller than those of the ASCC and PSCC. Each SCC formed a distorted circle because it ran into the vestibule. This distorted circle of the ASCC had the largest area and the longest perimeter (Table 1).

Table 1. Dimensions of the SCCs
 ASCCPSCCLSCC
MeanSDMeanSDMeanSD
  1. Unit: mm; Radius of curvature=0.5(height+width)/2.

  2. a

    Significant difference between males and females (P<0.05).

Height6.50.56.70.64.90.6
Width8.00.57.70.56.50.7
Radius of curvature3.60.23.60.22.90.3
Perimeter of distorted circle18.61.718.0a2.110.32.9
Area of distorted circle (mm2)24.34.219.6a4.07.53.1

The internal width and internal height of each SCC were measured at three points from the distal common crus to the proximal common crus. The internal widths of the ASCC and PSCC were similar, while the LSCC was wider than the other SCCs. In terms of the internal height, the middle points of the ASCC and LSCC were slightly higher than their distal and proximal points. However, the internal height of the PSCC was the same at these three points (Table 2).

Table 2. Internal widths and internal heights of the SCCs
 ASCCPSCCLSCC
MeanSDMeanSDMeanSD
  1. Unit: mm; Dimensions labeled “1,” “2,” and “3” were measured at the distal common crus, between the distal and proximal common cruses, and at the proximal common crus, respectively.

Internal width 11.20.21.40.22.10.3
Internal width 20.90.21.50.21.70.3
Internal width 31.20.11.40.21.70.2
Internal height 11.00.11.00.11.20.2
Internal height 20.70.11.00.10.80.1
Internal height 30.90.10.90.11.20.3

The SCCs did not form exact 90-degree angles with each other in the present study: the angles between the ASCC and PSCC, ASCC and LSCC, and PSCC and LSCC were 92.1, 84.4, and 86.2 degrees, respectively (Fig. 2, Table 3).

Figure 2.

Examples of angles between the SCCs. A: Angles between the ASCC and PSCC. B: Angles between the ASCC and LSCC. C: Angles between the PSCC and LSCC.

Table 3. Angles between the SCCs
 MeanSDMinMax
  1. Unit: degrees.

ASCC–PSCC92.13.584.299.0
ASCC–LSCC84.44.274.689.9
PSCC–LSCC86.22.481.189.8

The length of the common crus was 2.0 mm. The width of the common crus was measured at three points: superior, middle, and inferior. The common crus was slightly thinner at the middle point but its width did not differ significantly between the superior and inferior point (Table 4).

Table 4. Length and width of the common crus
 LengthWidth 1Width 2Width 3
MeanSDMeanSDMeanSDMeanSD
  1. Widths labeled “1,” “2,” and “3” were measured at superior, middle, and inferior points.

Dimension (mm)2.00.51.60.31.50.31.90.4

DISCUSSION

The SCCs are among the most difficult anatomical structures to investigate due to their complicated 3D shape being embedded inside the dense otic capsule of the petrous bone (Spoor and Zonneveld, 1995). This has led to conventional CT images being used for measuring SCC dimensions. However, such images are inadequate since they are 2D, which makes it difficult to accurately characterize the very complicated 3D structure of the SCCs. Moreover, the intervals and pixel size of conventional CT images are too large to accurately measure SCC dimensions.

The height and width were measured for each canal and the radius of curvature was calculated in the present study. The canal shapes were roughly circular, and therefore simple radius-of-curvature measurements should be sufficient to characterize the canal size (Curthoys et al., 1977). Spoor and Zonneveld (1998) measured the sizes of the SCCs using CT images of 53 human temporal bones. The radius of curvature was largest for the PSCC (3.8 mm) in their study, while that of the ASCC and PSCC (3.6 mm) was similar in the present study.

The first item in adult cadaver that was not measured in the previous study (Spoor and Zonneveld, 1998) was the area of the distorted circle of the SCC. In the present study this dimension of the ASCC was about 1.2 and 3.2 larger than those of the PSCC and the LSCC, respectively. The area of the PSCC was about 2.6 greater than that of the LSCC. Traditionally the radius of curvature was considered to show the canal size, but the area of the circles of the SCCs also might be a suitable dimension for quantifying the canal size.

Animals having large SCCs are characterized by high locomotor agilities and rapid movements (Spoor et al., 2003; Welker et al., 2009). The sizes of the SCCs are related to the sensitivity or response time of locomotor behaviors (Spoor and Zonneveld, 1998). Because the size of each SCC differs in humans, it can be assumed that the response time and sensitivity differ between the SCCs.

It is generally considered that the SCCs are set at right angles to each other (Moore and Agur, 2011), but the canals did not form precise right angles in the present study. In most of the specimens the ASCC made an obtuse angle with the PSCC (75%; 30 of 40 cases). However, the angles between the other two SCCs (ASCC–LSCC and PSCC–LSCC) were acute in all specimens. Unlike when using a 2D image, it was easy to measure the angle between SCCs in the 3D space because the specimen could be rotated and directly measured using the computer software.

Many studies of the inner ear have used 3D reconstruction (Wang et al., 2007; Trier et al., 2008; Sørensen et al., 2009; Teranishi et al., 2009; Welker et al., 2009; Bloch and Sørensen, 2010; Jang et al., 2011), and a 3D simulator has been used for visualization in surgical procedures involving the middle ear or inner ear (Wang et al., 2007; Trier et al., 2008; Sørensen et al., 2009). Such a 3D simulator was considered very useful for otology surgeons because the structures of the ear could be gradually shown from the external ear to the inner ear using a “drilling” tool, thereby clearly representing the relationship between the inner ear and peripheral structures. However, those studies focused on the process of simulator development for use as a training reference for approaches during ear surgery, and not on the structure of the inner ear itself.

Teranishi et al. (2009) compared the endolymphatic and perilymphatic spaces of the bony labyrinth in temporal bones with and without endolymphatic hydrops using 3D reconstruction. The temporal bone was sectioned at a thickness of 20 µm, and 3D reconstruction of the inner ear was performed through segmentation of the endolymphatic and perilymphatic spaces. Although they obtained clear images of the SCCs and could distinguish the endolymphatic and perilymphatic spaces, the acquisition of histological sections required a highly skilled technique. In addition, the decalcification and other histological processes resulted in distortion of even the normal specimens. Bloch and Sørensen (2010) provided inner ear images of otosclerosis patients and the 3D location and shape of otosclerotic lesions. A high-resolution 3D model of the inner ear was constructed, which revealed the positional relationship of the SCCs, cochlea, and facial nerve. However, their measurements could not accurately reflect the real inner ear because of distortion due to histological processes such as decalcification and staining. In the present study, the 3D reconstruction using micro-CT images of the temporal bone was convenient, time-saving, and allowed various dimensions to be measured directly using software.

Aplasia or hypoplasia of the LSCC was observed in two of our cases (Fig. 3). Deformation of the LSCC was evident on the left and right sides of the same cadaver (a 23-year-old male). Both ASCCs were smaller than normal and the common cruses were very thin. The LSCC is the last of the SCCs to complete ossification and is the most susceptible to anomalous development (Brookhouser, 1993). Disturbance of normal fusion and ossification may lead to a short LSCC complex or to a persistent anlage-type configuration of the LSCC with the absence of a central ossified bony island (Harada and Sando, 1981; Satar et al., 2003; Yu et al., 2003). Inner ear malformations were traditionally thought to be associated with sensorineural hearing loss (Yamashita et al., 2011), but the relationship between LSCC dysplasia and sensorineural hearing loss is controversial (Johnson and Lalwani, 2000; Mafong et al., 2002; Purcell et al., 2006; Simons et al., 2006; Dallan et al., 2008; Yukawa et al., 2008). The SCCs and vestibule are involved in balance (Moore and Agur, 2011), with the utricle and saccule responding to linear acceleration (e.g., turning the head to the left or right) and the orientation of the head relative to gravity (e.g., tilting the head to the left or right). The LSCC plays a role in the vestibulo-ocular reflex, which allows the gaze to remain fixed on an object while the head is moving (e.g., trying to read a sign in a moving car). The lack of pre mortem medical records in the present study made it impossible to confirm if equilibrium dysfunction had resulted from the abnormal LSCCs. Described above, in our opinion the balance function of the subject would have been normal due to adaptation assistance from the other SCCs and the normal utricle and saccule.

Figure 3.

Deformation of the LSCC. A: Aplasia and B: Hypoplasia of the LSCC were present in the same cadaver.

The present study has provided a high-resolution 3D model of the SCCs that overcomes major limitations of previous studies that used conventional CT images and various 3D reconstruction techniques. Accurate knowledge of the dimensions of the SCCs obtained using 3D reconstruction from micro-CT images of the inner ear could represent very important reference data for otology surgeons.

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