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Microcomputed tomography of the stapes: Wide-ranging dimensions.

Abstract

Although human stapes are known to have varied dimensions and the footplate is considered to be oval (fitting as it does into the oval window), few studies of high-resolution imaging of these structures have been performed. No study appears to have addressed the bilateral symmetry of stapes dimensions or to have determined if an association exists between the size of the stapes and the size of mastoid pneumatization; a small mastoid pneumatization is an indicator of childhood otitis media. We obtained 41 ear-normal cadaver crania specimens for study in our temporal bone laboratory and isolated 10 for further analysis: the 5 with the largest areas of mastoid pneumatization and the 5 with the smallest. Microcomputed tomography of tissue blocks was performed on the in situ stapes. Using Image] software, we created a three-dimensional model of each stapes. The mean height of these stapes was 3.43 mm (range: 3.20 to 3.80), the mean length of the footplates was 2.71 mm (range: 2.52 to 2.97), and the mean width of the footplates was 1.23 mm (range: 1.12 to 1.46). Qualitatively, the footplate was shaped like a human footprint in moist sand, as Eysell described in 1870. The dimensions of the stapes were found to be bilaterally symmetrical in general, but there was no correlation between these dimensions and the size of mastoid pneumatization. The distribution of footplate widths may be bimodal, which is consistent with the observation of Sim et al that men have wider footplates than do women.

Introduction

The stapes, the smallest of all the named bones in the human body, has intrigued clinicians and researchers for many years. More than a century ago, Eysell (1) and Urbantschitsch (2) published qualitative and quantitative descriptions of the stapes. Dass et al in 1966 reported marked variations in stapedial structure. (3) Working with a precision caliper under a microscope, aWengen et al found an impressive range of distances in six measurements between various points on the stapes. (4) Rouset et al, studying normal ears with clinical computed tomography (CT), found that stapes heights ranged from 2.3 to 4.2 mm (mean: 3.7). (5)

Using microcomputed tomography (microCT), Sim et al reported stapes heights and footplate lengths and widths as 3.28 ([+ or -]0.21), 2.81 ([+ or -]0.16), and 1.27 ([+ or -]0.11) mm, respectively, in predominately right-sided stapes. (6) They also reported that men have wider footplates than do women.

In this article, we describe our study to validate the work of Sim et al, (6) as well as to assess bilateral symmetry in the quantitative features in pairs of stapes and to determine the qualitative appearance of the footplates. Our hypothesis was that there is symmetry between the stapes pairs--a feature that to the best of our knowledge has not been previously studied. Bilateral symmetry would suggest that genetic influences play a role in stapes development.

A secondary aim of our investigation was to correlate stapes metrics with mastoid pneumatization (minimal temporal bone pneumatization is a correlate of childhood otitis media). (7,8) Our hypothesis was that the development of the stapes is independent of the size of mastoid pneumatization. To the best of our knowledge, this issue has not been explored, either.

A third goal was to determine if stapes height, footplate width, and footplate length are correlated. In other words, If a stapes is large in one dimension, is it large in the other dimensions, as well, and vice versa? The question is apropos, since Rodriguez-Vazquez reported that the entire stapes develops from the mesenchyme of the second branchial arch, independent of both the Reichert cartilage and the otic capsule. (9)

Finally, a fourth objective was to determine if the distribution of footplate widths is bimodal, since Sim et al reported that footplates are wider in men than in women. (6)

Materials and methods

Specimens. We studied 41 adult skulls (82 temporal bones) that were provided by the anatomy unit at the Emory University School of Medicine. The specimens had been obtained from humans who had bequeathed their bodies to science before they died. No information about the age, sex, and race/ethnicity of the donors was available. While we knew that none of the donors had died of ear disease, further unambiguous historical ear data were not available.

On plain Law lateral radiography of the 82 temporal bones, the areas of mastoid pneumatization were traced as previously described. (10) The 5 crania with the largest areas of mastoid pneumatization and the 5 with the smallest underwent microCT imaging.

MicroCT and 3-D reconstruction. Images of the 20 temporal bones from the 10 selected crania were obtained on a microCT device (Inveon MicroCT; Siemens Healthineers; Erlangen, Germany). Since the gross physical sizes of the temporal bones exceeded the imaging aperture of the scanner, the specimens were physically reduced. The microCT images were then made with a pixel size of 20 x 20 [micro]m, a slice thickness of 21.5 and a resolution of 46.499 pixels/mm.

Segmentation and 3-D volume reconstruction were performed with the ImageJ program and the plug-in Bone J. (11,12) First, each stapes was cropped from the surrounding structures and ambient air by hand. Second, the "background noise" was subtracted. Third, the image stack was processed with the Isosurface algorithm of BoneJ, which converts the stack into a triangular surface model. The surface model was saved into a Standard Tessellation Language (STL) file format for dimensional analysis of the stapes structure. Fourth, the 3-D viewer was used to visualize the STL models. Reference points were marked directly on the 3-D models and recorded as x, y, and z coordinates.

Complete stapes were missing from 2 tissue blocks before microCT imaging, and therefore no data were obtained from them. For 2 other stapes, the crura were damaged before microCT imaging, making calculation of stapes height impossible.

Stapes measurements. The stapes height was calculated by measuring the distance between a point in the center of the top of the capitulum and a point in the center of the stapes footplate on the medial (vestibular) surface (figure 1). The footplate's length was calculated by measuring the distance between points on both ends of the long axis of the footplate annulus. The footplate's width was calculated by measuring points on both ends of the short and long axes of the footplate annulus.

After we created the models in BoneJ, we identified each landmark in 3-D space (x, y, and z) with the point tool. For measurements of the footplate length, we used the landmarks that represented the farthest point on the "big toe" side of the footplate and the farthest point at the "heel." For footplate width, we determined the widest diameter perpendicular to the footplate length. Footplate dimensions were thus determined in a manner analogous to a shoe salesman measuring a foot (figure 2).

Each measurementwas performed twice, independently.

Calculations and statistics. Distance measurements were calculated according to the Pythagorean theorem in three dimensions. Only ifassociations were suggested on scatterplot graphs were nonparametric Spearman correlations calculated. No correction for multiple comparisons was done.

Ethical considerations. Our university's Institutional Review Board determined that IRB approval was not required because this study "does not meet the definition of'research involving human subjects' or the definition of clinical investigation' under applicable federal regulations."

Results

The range of stapes heights was wide (3.20 to 3.80 mm; mean: 3.43), as were the ranges of footplate lengths (2.52 to 2.97 mm; mean: 2.71) and widths (1.12 to 1.46 mm; mean: 1.23). The repeatability of measurements was excellent (table).

Bilateral symmetry of the stapes measurements was suggested, but symmetry was statistically significant only for the footplate width ([r.sub.s] = 0.86; n = 8; 95% confidence interval: 0.39 to 0.97). No stapes feature showed a correlation with the size of mastoid pneumatization.

We found no correlation among the linear dimensions themselves--that is, if anyone measured dimension of a stapes was small (or large), other measured dimensions of that stapes were not necessarily small (or large).

Unlike the distribution of the stapes height and footplate length, the distribution of footplate width maybe bimodal (figure 3).

Each footplate qualitatively resembled the appearance of a sock-covered human foot.

Discussion

The stapes measurements acquired in this study are consistent with those of previous reports. (2-4,6) The mean height, footplate length, and footplate width for combined right and left stapes in our study was 3.43, 2.71, and 1.23 mm, respectively. Sim et al demonstrated similar findings using micro-CT analysis. (6) They also reported that men have wider footplates than women (mean: 1.32 vs. 1.17 mm, p < 0.001).

Our study aimed to overcome a limitation ofprevious microCT analyses by looking at pairs of stapes. Bilateral symmetry was suggested for all three metrics, but because of the small number of specimens, we found statistical significance only with respect to footplate width.

No correlation of the stapes parameters and the size of mastoid pneumatization was suggested. Thus, these data may indicate that local middle ear environmental factors affecting pneumatization are unrelated to stapes development. The first and second branchial arches and the first pouch contribute to the development of the middle ear. Mastoid bone development occurs at a very different stage of life, but it might nevertheless be influenced by "intrinsic defects." (13) The fact that we did not find a correlation between stapes height and footplate length and width might be surprising, considering the second arch one-anlage origin of the entire stapes. (9)

The major limitations of our study are that (1) we looked at specimens of only 10 crania (the 5 with the largest areas of mastoid pneumatization and the 5 with the smallest) and (2) we had no specific information about age, sex, or otologic history. Nevertheless, our study does have three distinct positive features: (1) the specimens represented the size extremes of mastoid pneumatization in 41 clinically ear-normal crania, (2) images of the stapes were obtained in situ, and thus any possible damage sustained during harvesting was precluded, and (3) bilateral symmetry of stapes features was checked.

In conclusion, stapes heights and footplate lengths and widths in our study were consistent with those reported by Sim et al (6) and others. (2-4) Studying as few as 7 paired specimens, we found that bilateral symmetry was suggested for superstructure height and footplate length and found to be statistically significant for footplate width. We found no correlation between the stapes measurements and the size of mastoid pneumatization. The distribution of footplate widths may be bimodal, as reported by Sim et al, in that men have wider footplates than do women. (6)

Jason Patrick Calligas, MD; Norman Wendell Todd Jr., MD, MPH

From the Department of Otolaryngology-Head and Neck Surgery, Emory University School of Medicine, Atlanta.

Corresponding author: Norman Wendell Todd Jr., MD, MPH, Emory Children's Center, 2015 Uppergate Dr., NE, Atlanta, GA 30329. Email: ntodd@emory.edu

References

(1.) Eysell A. Beitrage zur Anatomie des Steigbugels und seiner Verbindungen. Arch Ohrenheilk 1870;5:237-49.

(2.) Urbantschitsch V. Zur anatomie der Gehorknochelchen des Menschen. Arch Ohrenheilkunde 1876;11:1-10.

(3.) Dass R, Grewal BS, Thapar SP. Human stapes and its variations. I. General features. I Laryngol Otol 1966;80(1):11-25.

(4.) aWengen DF, Nishihara S, Kurokawa H, Goode RL. Measurements of the stapes superstructure. Ann Otol Rhinol Laryngol 1995;104(4 Pt 1):311-16.

(5.) Rousset J, Garetier M, Gentric JC, et al. Biometry of the normal stapes using stapes axial plane, high-resolution computed tomography. J Laryngol Otol 2014;128(5):425-30.

(6.) Sim JH, Roosli C, Chatzimichalis M, et al. Characterization of stapes anatomy: Investigation of human and guinea pig. J Assoc Res Otolaryngol 2013;14(2):159-73.

(7.) Swarts JD, Foley S, Alper CM, Doyle WJ. Mastoid geometry in a cross-section of humans from infancy through early adulthood with a confirmed history of otitis media. Int J Pediatr Otorhinolaryngol 2012;76(1): 137-41.

(8.) Chole RA, Sudhoff HH. Chronic otitis media, mastoiditis, and petrositis. In: Flint PW, Haughey BH, Lund VJ, et al, eds. Cummings Otolaryngology: Head and Neck Surgery. 6th ed. Philadelphia: Elsevier Saunders; 2014:1965-78.

(9.) Rodriguez-Vazquez JF. Development of the stapes and associated structures in human embryos. J Anat 2005;207(2):165-73.

(10.) Todd NW. Orientation of the manubrium mallei: Inexplicably widely variable. Laryngoscope 2005;115(9):1548-52.

(11.) Doube M, Klosowski MM, Arganda-Carreras I, et al. BoneJ: Free and extensible bone image analysis in ImageJ. Bone 2010;47(6):1076-9.

(12.) Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 2012;9(7):671-5.

(13.) Kalter H. Teratology in the Twentieth Century Plus Ten. New York: Springer; 2010.

Caption: Figure 1. MicroCT shows a right stapes viewed from a surgeons perspective, laterally onto the superstructure. Note the footplate's socked-foot appearance, with the big toe anterorinferior. The red circle (1) indicates the center of the top of the capitulum.

Caption: Figure 2. MicroCT demonstrates a right footplate viewed onto the vestibular (medial) surface. The red circles denote the center of the footplate (2), the limits of its length (3), and the limits of its width (4) perpendicular to the length.

Caption: Figure 3. Chart shows that the distribution of footplate widths appears to be bimodal, consistent with two populations (presumably male and female, according to the work of Sim et al (6)).
Table. Summary of the repeatability and distribution of each
measurement *

                                         Repeatability,
Measurement                            [r.sub.s], (95% CI)

Mastoid area, right, all crania   0.89, n = 41, (0.80 to 0.94)

Mastoid area, left, all crania    0.92, n = 41, (0.85 to 0.95)

Height of stapes, right            0.99, n = 7, (0.93 to 0.99)

Height of stapes, left             0.99, n = 9, (0.95 to 0.99)

Length of footplate, right         0.80, n = 9, (0.21 to 0.96)

Length of footplate, left         0.87, n = 10, (0.86 to 0.99)

Width of footplate, right          0.87, n = 8, (0.42 to 0.98)

Width of footplate, left          0.96, n = 10, (0.86 to 0.99)

                                          Repeatability,
Measurement                                 practical

Mastoid area, right, all crania        31/41, [less than or
                                      equal to] 2 [cm.sup.2]

Mastoid area, left, all crania    34/41 [less than or equal to]
                                           2 [cm.sup.2]

Height of stapes, right                 5/7 [less than or
                                        equal to] 0.05 mm

Height of stapes, left                  7/10 [less than or
                                        equal to] 0.05 mm

Length of footplate, right              6/8 [less than or
                                        equal to] 0.05 mm

Length of footplate, left               6/10 [less than or
                                        equal to] 0.05 mm

Width of footplate, right               5/8 [less than or
                                        equal to] 0.05 mm

Width of footplate, left                9/10 [less than or
                                        equal to] 0.05 mm

Measurement                               Median (range)

Mastoid area, right, all crania    9.6 [cm.sup.2] (2.4 to 14.2)

Mastoid area, left, all crania    10.0 [cm.sup.2] (2.0 to 18.0)

Height of stapes, right               3.30 mm (3.20 to 3.80)

Height of stapes, left                3.45 mm (3.25 to 3.74)

Length of footplate, right            2.71 mm (2.62 to 2.97)

Length of footplate, left             2.68 mm (2.52 to 2.83)

Width of footplate, right             1.20 mm (1.13 to 1.46)

Width of footplate, left              1.22 mm (1.12 to 1.33)

* Repeatability is depicted by both the Spearman nonparametric
correlation coefficient [r.sub.s], with 95% confidence interval
(CI), and by a clinically relevant value. Each measurement
represents the mean of two independent measurements.
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Title Annotation:ORIGINAL ARTICLE
Author:Calligas, Jason Patrick; Todd, Norman Wendell, Jr.
Publication:Ear, Nose and Throat Journal
Article Type:Report
Date:Apr 1, 2018
Words:2628
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