Computed Tomographic Features of the Osseous External Ear Canal, Tympanic Membrane, and Tympanic Bulla in Clinically Normal Horses

Accepted Manuscript Computed tomographic features of the osseous external ear canal, tympanic membrane and tympanic bulla in clinically normal horses Annemarie Blanke, Stefanie Ohlerth, Josef Hollerrieder, Gerald Fritz Schusser PII:

S0737-0806(16)30019-3

DOI:

10.1016/j.jevs.2016.03.001

Reference:

YJEVS 2046

To appear in:

Journal of Equine Veterinary Science

Received Date: 22 January 2016 Accepted Date: 3 March 2016

Please cite this article as: Blanke A, Ohlerth S, Hollerrieder J, Schusser GF, Computed tomographic features of the osseous external ear canal, tympanic membrane and tympanic bulla in clinically normal horses, Journal of Equine Veterinary Science (2016), doi: 10.1016/j.jevs.2016.03.001. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

ACCEPTED MANUSCRIPT

Computed tomographic features of the osseous external ear canal,

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tympanic membrane and tympanic bulla in clinically normal horses

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Annemarie Blankea, Stefanie Ohlerthb, Josef Hollerriederc and Gerald Fritz

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Schussera*

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a

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Leipzig, Germany

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[email protected]; [email protected]

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b

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Department of Large Animal Medicine, Faculty of Veterinary Medicine, University of

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Clinic of Diagnostic Imaging, Vetsuisse Faculty, University of Zurich, Switzerland

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[email protected]

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[email protected]

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*Corresponding author:

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Prof. Dr. Dipl. ECEIM Gerald F. Schusser

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Department of Large Animal Medicine, Faculty of Veterinary Medicine, University of

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Leipzig, Germany

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An den Tierkliniken 11

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04103 Leipzig, Germany

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Tel.: 0049 341 97 38 320

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Fax: 0049 341 97 38 349

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E-mail: [email protected]

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Tieraerztliche Klinik Domaene Karthaus, Duelmen, Germany

ACCEPTED MANUSCRIPT Abstract

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Only sparse anatomical and morphometric information exists concerning the equine

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acoustic organ. The aim of the present study was, therefore, to describe the

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computed tomographic (CT) anatomy and determine the CT dimensions of the

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osseous external ear canal (OEEC), tympanic membrane (TM) and tympanic bulla

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(TB) in clinically normal horses.

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Computed tomography of the head was performed in 23 horses, presented for

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reasons unrelated to the auditory organ, with a 4-slice (group 1) or a 40-slice (group

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2) CT scanner, respectively. The following measurements of the OEEC were

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performed: volume, dorsal, ventral and central length, half-way of central length and

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inner diameter at four different locations. Length of the TM, width of the

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hypotympanon and the largest width and height of the external acoustic porus (EAP)

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and the TB were also recorded.

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The OEEC in all ears was of an oval, truncated cone shape running in a dorsolateral

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to medioventral direction. The TM coursed at a flat angle from dorsolateral to

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medioventral and had a wave-like appearance on transverse CT images.

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Significantly lower width and height of the EAP, inner diameter of the OECC at its

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narrowest point and OEEC volume was found in group 1. A significant positive

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correlation between OEEC volume and head length or body weight, respectively, was

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found in group 2.

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Results of the present study may serve as reference values and aid the diagnosis of

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aural abnormalities and disease conditions. Moreover, they provide a basis for the

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adjustment of audiometric testing devices to horses.

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Keywords:

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External ear canal

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Tympanic bulla

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Tympanic membrane

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Computed tomography

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Horse

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ACCEPTED MANUSCRIPT 1. Introduction

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Computed tomography (CT) has been proven an excellent technology for the

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investigation of the normal anatomy and geometry of the auditory organ [1-3], as well

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as middle and inner ear diseases in humans and small animals [4-7]. Computed

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tomography reference values for external and middle ear structures were reported in

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detail for a sample of normal llamas [8] and, so far, only in one dissected normal

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equine head [9]. However, knowledge about the CT anatomy and dimensions of the

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equine auditory organ could prove useful for the diagnosis of aural malformations

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and diseases. It may also provide a basis for the adjustment of human audiometric

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testing devices (measurement of otoacoustic emissions, tympanometry) for horses.

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In particular, the size and shape of the external ear canal (EEC) influence

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transmission of sound waves and, finally, determine sound pressure at the tympanic

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membrane (TM) [10]. Geometrical dimensions of the EEC (length, radii, shape and

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volume) vary significantly among species and, therefore, influence audiometric

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measurements. Otoacoustic emission in cats, for example, can be measured twice

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as fast as in human ears due to the smaller volume of the feline EEC [11].

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Equine ear diseases have been reported infrequently in the past. Diseases mainly

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related to the external ear, such as polyps, othematoma, chondrosis, plaques,

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parasites (ticks, mites and culicoides), aural foreign bodies and various stages of

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otitis externa, have been described previously [9,12-17]. Examination of the equine

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ear is also part of the work-up of headshaking, temporohyoid osteoarthropathy,

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vestibular disease, facial nerve paralysis and head trauma [9,16-19]. However,

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otoscopic examination is challenging in the horse due to difficulties in visualizing the

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EEC and the TM. Patient compliance is often poor. A recent report described the

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usefulness of veterinary video endoscopes for the otoscopic examination in sedated

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standing horses [17].

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ACCEPTED MANUSCRIPT 80

The aim of the present study was to describe the anatomy and determine the

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dimensions of the osseous EEC (OEEC), TM and tympanic bulla (TB) in clinically

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normal horses with CT.

83 2. Materials and methods

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2.1. Animals

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Computed tomography scans of 23 equine patients (46 ears) were included in the

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study between March 2013 and April 2014. Horses underwent CT because of

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diseases unrelated to the auditory organ (e.g. dental disease, sinusitis, ethmoid

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hematoma, idiopathic headshaking, retrobulbar mass, brain tumor, laryngeal

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disease). Animals were included only if 1) body weight was between 400 and 700 kg,

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2) signs of aural diseases were absent during clinical examination, and 3) the CT

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scan of the ears was considered normal. The study sample comprised 19 warm-

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blooded horses of various breeds, one Quarter Horse and three Arabian horses; 13

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were male and 10 were female.

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2.2. CT examination

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A 4-slice1 and a 40-slice CT scanner2 were used in 10 (group 1) and 13 (group 2)

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horses, respectively. All horses were under general anesthesia and positioned in

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dorsal recumbency to obtain transverse contiguous slices. Settings for group 1 were:

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120 KV, 200 mAs, 0.75 s tube rotation, pitch of 1, increment of 1 mm and 2 mm slice

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collimation. Settings for group 2 were: 140 KV, 300 mAs, 1 s tube rotation, pitch of

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0.55, increment of 1.2 mm and 3 mm slice collimation. The CT data was

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reconstructed to images with 2 mm (group 1) and 0.6 mm (group 2) slice thickness

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using a medium frequency image reconstruction algorithm (soft tissue) and a high-

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frequency image reconstruction algorithm (bone), respectively. A board-certified

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ACCEPTED MANUSCRIPT radiologist (SO) and the first author (AB) reviewed all CT images with dedicated

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software using multiplanar and 3D reconstruction modes3. A bone window was

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applied for the assessment of the OEEC and TB (window width, 3000 Hounsfield

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units; window level, 400 Hounsfield units). Window settings were minimally adapted

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for the evaluation of the TM.

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111 2.3. Measurements on CT images

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Measurements of the skull were performed to address individual differences.

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Because the brain was not included in the scan field in group 1, only the head length

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was measured in group 2 and defined as the distance from the rostral border of the

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palatine process to the external occipital protuberance on sagittal CT images at the

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level of the nasal septum. On a transverse CT image at the level of the OEEC, the

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head height was obtained in both groups by measuring the distance from the dorsal

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internal cortex of the skull, at the level of the sagittal crest, to the internal cortex of

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the base of the basisphenoid.

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Measurements of the right and left ear were obtained in every horse. The length of

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the OEEC was assessed on a transverse CT image in which it was visible at its

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maximal length and width (Figure 1). Its ventral length (Lv) and dorsal (Ld) length

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was measured along the ventral and dorsal wall from the external acoustic porus

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(EAP) to the ventral or dorsal aspect of the TM, respectively. Additionally, the central

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length (Lc) was determined along a central line from the midpoint of the TM (MPTM)

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to the midpoint of the EAP (MPEAP). On the same transverse image, the length of

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the TM (LTM) was also measured along its course. Furthermore, the inner diameter

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of the OEEC was determined at four different locations: at the EAP from its dorsal to

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ventral aspect (DEAP), half-way of the central length (DCL1/2), at the narrowest point

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of the OEEC (DNP), and at the tympanic annulus (TA) from its dorsal to ventral

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ACCEPTED MANUSCRIPT aspect (DTA). The diameters DCL1/2 and DNP were measured at a 90° angle to the

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dorsal wall. Finally, the width of the hypotympanon (WHT), as well as the largest

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width (WB) and height of the TB (HB) were obtained on the same transverse image.

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The largest height (HEAP) and width (WEAP) of the EAP was determined on sagittal

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CT images. The volume of the OEEC was determined by delineating the inner cross-

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sectional area of the OEEC on every sagittal image from the EAP to the TA; volume

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was calculated electronicallyc.

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All statistical analyses were performed using a commercial software package4.

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Firstly, continuous variables were tested for normal distribution with the Kolmogorov-

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Smirnoff test. Differences between left and right ear, gender and groups (1, 2) were

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analyzed by means of a two-tailed paired t-test and an independent samples t-test,

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respectively. Pearson’s correlation coefficients were calculated to analyze

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associations between all CT variables and body weight. A p-value ≤ 0.05 was

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considered significant.

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3. Results

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The osseous and soft tissue structures of the equine ear were generally very well

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depicted with CT. However, full depiction of small structures, such as the TM, the

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ossicles’ chain (malleus, incus, stapes) and tensor tympani muscle, was difficult and

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not always possible in group 1, whereas their visibility was considered markedly

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superior in group 2.

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The OEEC in all ears represented a continuation of the cartilaginous EEC running in

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the same oblique dorsolateral to medioventral direction. The TM also coursed in a flat

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angle from dorsolateral to ventromedial. It had a wave-like appearance on transverse

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ACCEPTED MANUSCRIPT CT images due to its central attachment at the malleus handle, which projected

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beyond the TA. The cross-sectional area of the auditory canal was of an oval shape

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in sagittal images, with the width being smaller than the height. The inner diameter of

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the OEEC decreased markedly from lateral to medial. The shape of the OEEC

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resembled a narrowing tube (Figure 2).

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Results of the descriptive statistics are shown in Table 1. Mean values did not

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significantly differ between gender and ear. However, DNP, HEAP, WEAP and

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volume of the OEEC were significantly lower in group 1 (p = 0.016, 0.007, 0.030 and

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0.019, respectively). A significant positive correlation between the volume of the

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OEEC and body weight (p = 0.021, r = 0.638) or head length (p = 0.002, r = 0.771)

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was found in group 2; significance disappeared if the three Arabian horses were

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excluded. Unfortunately, exact body weight was not available for horses in group 1.

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No significant association was found between head height and the volume of the

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OEEC in either group. Otherwise, association between variables did not change

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independently whether the data of the Arabian horses were in- or excluded.

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4. Discussion

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One major goal of the present study was to describe the CT anatomy of the equine

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acoustic organ. The EEC in canine ears is divided into a vertical and horizontal part

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[20,21]. By contrast, the cartilaginous and osseous EEC in the present equine

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sample represented merging structures running in a continuous oblique dorsolateral

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to medioventral direction. The OEEC showed an oval, truncated cone shape, which

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is in contrast to the hourglass-shape described by Sargent et al. [9]. The equine TM

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coursed from dorsolateral to medioventral in a rather flat angle, in contrast to dogs

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and humans which had reported angles of 45° and 40 - 60°, respectively [22,23].

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Visibility of the TM was markedly superior on the thin slices (0.6 mm) in group 2.

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ACCEPTED MANUSCRIPT Slices thinner than 1 mm are mandatory for a reliable depiction [1]. However, CT

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units with a high number of detector rows are not routinely available in private equine

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clinics. The equine TB was relatively small with a simple architecture, in comparison

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to the relatively larger and more complex bullae in carnivores and ruminants [9,8,24].

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However, the maximum width and height of the TB ranged greatly between individual

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horses.

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The second goal of this study was to determine the dimensions of the OEEC, TM and

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TB in clinically normal horses. Results may not only serve as reference values in

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clinical cases, they may also provide a basis for the adjustment of human

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audiometric testing devices to horses. Therefore, the authors of the present study

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tried initially to transfer CT measurement techniques from humans to horses.

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Unfortunately, due to the typical s-shape of the human auditory canal, a recently

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published method to assess its length with high-resolution CT [1] was not applicable

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to the horse. In human ears, authors measured the distance from the innermost

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ventral tip of the TM to the second bend of the cartilaginous auditory canal [1]. The

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mean volume of the auditory canal in humans was 0.69 - 0.7 ml for the left and right

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ear [1].

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By contrast, the mean Ld of the OEEC in llamas measured 2.4 - 2.5 cm in males and

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females [8], which is much longer than in horses. In carnivores, one report published

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a mean length of the EEC (cartilaginous ear canal included) of 4.1 cm with a wide

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range [21]. Due to the inclusion of the cartilaginous ear canal, strong breed-specific

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differences in carnivores, and different measurement points and methods, a

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comparison to equine ears is difficult.

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ACCEPTED MANUSCRIPT Similarly in humans and llamas, there were no significant differences between left

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and right ears for all measurements. However, contrary to findings in humans [1] and

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llamas [8], gender differences were not found. The positive significant correlation

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between head length or body weight and the OEEC volume in group 2 disappeared if

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Arabian horses were excluded from the statistical analysis. This finding may indicate

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an influence of breed and should be taken into account when evaluating clinical

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cases or adjusting audiometric testing devices to horses. Nevertheless, results need

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to be confirmed in a larger cohort.

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A few measurements, such as DNP, HEAP, WEAP and volume of the OEEC, were

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significantly lower in group 1. Differences may be explained by the difference in slice

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thickness (group 1 = 2.0 mm; group 2 = 0.6 mm) and resulting volume averaging;

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however, due to a lack of data, influences such as body weight or head length cannot

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be ruled out.

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Knowledge of the shape, size and ear canal volume is essential for the adaption of

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audiometric testing devices to horses. It is well known from human studies that the

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acoustic input to the human auditory system is characterized by the reflection

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coefficient, sound intensity and forward sound pressure [25,26]. These factors are

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influenced by the anatomy of the OEEC. In particular, data regarding the volume of

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the OEEC is mandatory for adapting human objective auditory testing devices

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(tympanometry, measurement of otoacoustic emissions) to horses. In human

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neonates, the sound pressure level in front of the TM increases with decreasing

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OEEC volume [27,28]. Consequently, not only is the otoacoustic emission level

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higher, but sound is also transmitted faster in neonates than in adults [28]. Similar

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findings were made in cats, where the latency time needed to be reduced from 3.5

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ACCEPTED MANUSCRIPT 235

ms (human setting) to 1.5 ms to improve the recording of otoacoustic emission [11]. It

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might be reasonably assumed that latency time justifications are necessary when

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measuring otoacoustic emissions in horses.

238 5. Conclusions

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In the present study, species-specific anatomic features of the equine auditory organ

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were described and CT dimensions of the OEEC, TM and TB were determined in

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clinically normal horses. Established values may aid the diagnosis of aural

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abnormalities and disease conditions, and provide a basis for the adjustment of

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audiometric testing devices to horses. Breed-specific factors and CT properties

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should be taken into account.

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Acknowledgements

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The authors would like to thank the Hanns-Seidel-Stiftung e.V. for supporting A.

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Blanke with a doctoral scholarship.

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Footnotes

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1

SOMATOM Plus 4 Power, Siemens AG, Munich, Germany.

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2

SOMATOM Sensation Open, Siemens Schweiz AG, Zurich, Switzerland.

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3

OsiriX v.4.1.2. Foundation, Geneva, Switzerland.

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4

SPSS Statistics, Version 22, IBM, Chicago, Illinois, USA.

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der Audiometrie. 9th ed. Stuttgart, New York: Thieme; 2009, p. 113–36.

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ACCEPTED MANUSCRIPT Figure Legend

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Figure 1: Evaluated CT features of the osseous external ear canal (OEEC) and

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tympanic bulla (TB; transverse CT image of the left ear in a 15-year-old Hanoverian

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warmblood mare (0.6 mm slice thickness; WW: 3000 HU; WL: 400 HU)).

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Ld, dorsal length of the OEEC; Lv, ventral length of the OEEC; DEAP, diameter of

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the external acoustic porus (EAP); DEAP1/2, half-diameter of the EAP; DTA,

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diameter of tympanic annulus (TA); DTA1/2, half diameter of TA; LTM, length of the

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tympanic membrane (TM); 1, midpoint of the EAP (MPEAP); 2, midpoint of the TM

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(MPTM); Lc, central length; CL1/2, half of central length; DCL1/2, diameter half-way

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of central length; DNP, diameter at the narrowest point of the osseous ear canal;

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WHT, width of hypotympanon; WB, width of TB; HB, height of TB.

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Figure 2: Electronically reconstructed volume of the OEEC of a right equine ear

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(lateral view).

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1, lateral opening of the OEEC at the level of the EAP; 2, medial end of the OEEC at

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the level of the TM.

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Table 1: Descriptive statistics of the CT measurements in the normal OEEC and TB

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in 46 ears of 23 horses (group 1 = 20 ears of 10 horses examined with a 4-slice CT

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scanner; group 2 = 26 ears of 13 horses examined with a 40-slice CT scanner).

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Variable

Group 1:

Group 2:

Mean ± SD (Range)

Mean ± SD (Range)

Head height (cm)

8.69 ± 0.59 (7.74 – 9.53)

8.71 ± 0.60 (7.81 – 9.87)

Head length (cm)

Not available

53.44 ± 3.82 (47.37 – 57.62)

Ld (cm)

1.90 ± 0.10 (1.74 – 2.06)

1.81 ± 0.26 (1.25 – 2.20)

p-value

0.960

0.255

ACCEPTED MANUSCRIPT Group 2:

p-value

Mean ± SD (Range)

Mean ± SD (Range)

Lv (cm)

2.89 ± 0.15 (2.56 – 3.08)

2.76 ± 0.16 (2.51 – 2.97)

0.108

Lc (cm)

2.26 ± 0.13 (2.01 – 2.46)

2.20 ± 0.17 (1.93 – 2.47)

0.209

LTM (cm)

1.33 ± 0.12 (1.14 – 1.50)

1.31 ± 0.09 (1.16 – 1.42)

0.692

DEAP (cm)

1.20 ± 0.11 (0.99 – 1.41)

1.14 ± 0.11 (0.90 – 1.31)

0.141

DCL1/2 (cm)

0.50 ± 0.05 (0.41 – 0.57)

0.53 ± 0.05 (0.45 – 0.61)

0.063

DNP (cm)

0.42 ± 0.06 (0.32 – 0.50)

0.46 ± 0.04 (0.40 – 0.54)

0.016*

DTA (cm)

1.28 ± 0.11 (1.11 – 1.42)

1.23 ± 0.08 (1.08 – 1.33)

0.260

WHT (cm)

0.61 ± 0.07 (0.47 – 0.73)

0.63 ± 0.07 (0.51 – 0.77)

0.479

WB (cm)

1.31 ± 0.18 (1.06 – 1.55)

1.36 ± 0.30 (0.97 – 1.92)

0.745

HB (cm)

0.70 ± 0.11 (0.54 – 0.92)

0.73 ± 0.13 (0.55 – 1.08)

0.398

HEAP (cm)

0.80 ± 0.07 (0.69 – 0.92)

0.92 ± 0.11 (0.78 – 1.15)

0.007*

WEAP (cm)

0.65 ± 0.07 (0.55 – 0.77)

0.76 ± 0.09 (0.64 – 0.98)

0.030*

SC

RI PT

Group 1:

3

Volume (cm )

TE D

M AN U

Variable

3

0.384 cm ± 0.07 (0.27 –0.48)

3

0.486 ± 0.08 cm (0.35 – 0.62)

0.019*

Ld, dorsal length of the OEEC; Lv, ventral length of the OEEC; DEAP, diameter of

350

the EAP; DCL1/2, diameter half-way of central length; DNP, diameter at the

351

narrowest point of the OEEC; DTA, diameter of TA; LTM, length of the TM; Lc,

352

central length; WHT, width of hypotympanon; WB, width of TB; HB, height of TB;

353

HEAP, height of the EAP; WEAP, width of the EAP; *, significant differences between

354

measurements of group 1 and 2.

AC C

355

EP

348 349

ACCEPTED MANUSCRIPT Table 1

Group 1:

Group 2:

Mean ± SD (Range)

Mean ± SD (Range)

Head height (cm)

8.69 ± 0.59 (7.74 – 9.53)

8.71 ± 0.60 (7.81 – 9.87)

Head length (cm)

Not available

53.44 ± 3.82 (47.37 – 57.62)

Ld (cm)

1.90 ± 0.10 (1.74 – 2.06)

1.81 ± 0.26 (1.25 – 2.20)

0.255

Lv (cm)

2.89 ± 0.15 (2.56 – 3.08)

2.76 ± 0.16 (2.51 – 2.97)

0.108

Lc (cm)

2.26 ± 0.13 (2.01 – 2.46)

2.20 ± 0.17 (1.93 – 2.47)

0.209

LTM (cm)

1.33 ± 0.12 (1.14 – 1.50)

1.31 ± 0.09 (1.16 – 1.42)

0.692

DEAP (cm)

1.20 ± 0.11 (0.99 – 1.41)

1.14 ± 0.11 (0.90 – 1.31)

0.141

DCL1/2 (cm)

0.50 ± 0.05 (0.41 – 0.57)

0.53 ± 0.05 (0.45 – 0.61)

0.063

DNP (cm)

0.42 ± 0.06 (0.32 – 0.50)

0.46 ± 0.04 (0.40 – 0.54)

0.016*

DTA (cm)

1.28 ± 0.11 (1.11 – 1.42)

1.23 ± 0.08 (1.08 – 1.33)

0.260

WHT (cm)

0.61 ± 0.07 (0.47 – 0.73)

0.63 ± 0.07 (0.51 – 0.77)

0.479

WB (cm)

1.31 ± 0.18 (1.06 – 1.55)

1.36 ± 0.30 (0.97 – 1.92)

0.745

HB (cm)

0.70 ± 0.11 (0.54 – 0.92)

0.73 ± 0.13 (0.55 – 1.08)

0.398

0.80 ± 0.07 (0.69 – 0.92)

0.92 ± 0.11 (0.78 – 1.15)

0.007*

0.65 ± 0.07 (0.55 – 0.77)

0.76 ± 0.09 (0.64 – 0.98)

0.030*

HEAP (cm)

AC C

WEAP (cm)

3

Volume (cm )

p-value

3

0.384 cm ± 0.07 (0.27 –0.48)

0.960

RI PT

SC

M AN U

EP

TE D

Variable

3

0.486 ± 0.08 cm (0.35 – 0.62)

0.019*

AC C

EP

TE D

M AN U

SC

RI PT

ACCEPTED MANUSCRIPT

AC C

EP

TE D

M AN U

SC

RI PT

ACCEPTED MANUSCRIPT

ACCEPTED MANUSCRIPT 1

Computed tomographic features of the osseous external ear canal,

2

tympanic membrane and tympanic bulla in clinically normal horses

3

Annemarie Blanke, Stefanie Ohlerth, Josef Hollerrieder and Gerald Fritz Schusser

4

6

Highlights •

RI PT

5

The wave-like tympanic membrane coursed in a flat angle from dorsolateral to ventromedial.

7 •

The 3-D shape of the osseous external ear canal was an oval, truncated cone.

9

•

Visibility of small structures was improved with 0.6 mm slice thickness.

10

•

Volume of the osseous external ear canal may be influenced by breed and

Determined reference values may aid diagnosis of aural diseases and

EP

TE D

adjustment of audiometric devices.

AC C

13

•

M AN U

body weight.

11 12

SC

8