South American camelids such as llamas commonly develop otitis media secondary to upper respiratory tract infections,1 otitis externa, or intraaural foreign bodies. The predisposition of llamas for development of these infections may relate to anatomic factors, such as a long, narrow external acoustic meatus and a multi-compartmental tympanic bulla. These same factors complicate diagnosis. The external auditory meatus and osseous ear canal are narrow and undergo several direction changes, precluding consistent otoscopic evaluation of the deepest part of the canal and the tympanic membrane.2 In llamas, the tympanic bulla is large and honeycombed and lacks a fundic cavity, making radiographic evaluation difficult. For these reasons, ear infections in camelids are often not diagnosed until they are chronic and advanced and frequently not before they have led to cranial nerve dysfunction.3
Newer cross-sectional imaging techniques offer alternatives to otoscopy or conventional radiography for the diagnosis of otitis. Computed tomography and magnetic resonance imaging have both been used successfully to evaluate the external and middle ear in several species, including camels,4 dogs,5,6 California sea lions,7 and humans.8–10 Computed tomography has also been used successfully in the diagnosis of otitis media and interna in humans and a variety of other species, including dogs.5,8,9 These techniques allow evaluation of internal structures without interference of the narrowness of the canal or superimposition with overlying structures; they also allow detection of subtle changes in structures, which may lead to earlier diagnosis of disorders such as otitis. However, detailed description of the anatomic features of the ear of New World camelids is lacking. The purpose of the study reported here was to evaluate the osseous structures of the external acoustic meatus, tympanic cavity, and tympanic bulla of llamas without ear disease by use of CT and establish measurement values for those structures, thereby potentially aiding diagnosis of otic abnormalities and disease conditions in this species.
Materials and Methods
The heads of 10 healthy llamas (Lama glama) euthanized for meat production by use of a captive bolt striking the dorsal aspect of the skull were collected. None of the animals (6 males and 4 females) had abnormalities of the external ear or surrounding tissue. Each head was separated from the neck at the level of the atlantoaxial joint before the head was scanned and dissected. All heads were labeled at the right ear. For males, heads were labeled with the letter M and consecutive numbers (ie, M1 to M6); for females, heads were labeled with the letter F and consecutive numbers (ie, F1 to F4). Nine of the heads had permanent molars and were therefore considered to be from fully mature adult animals. Female 2, in which the last molar was in the process of eruption, was considered approximately 4 years old.11
Each head was scanned by use of a 64-slice CT scannera with slices acquired every 1 mm. The heads were positioned perpendicular to the scanner, with the hard palate parallel to the scanning table. Transverse images and sagittal and dorsal reconstructed images were evaluated at a window width of 2,700 Hounsfield units and a window level of 480 Hounsfield units.
Measurements on CT images—Each llama ear was divided into 3 major areas for obtaining measurements: the osseous external acoustic meatus, the tympanic cavity, and the tympanic bulla. Measurements of the right and left ear of each head were obtained on selected transverse, sagittal, and dorsal CT images (Figure 1) by use of commercially available software.b
Representative dorsal (A), transverse (B), and sagittal (C) CT images of the disarticulated head of an adult llama used in a study to evaluate and measure the osseous structures of the external acoustic meatus, tympanic cavity, and tympanic bulla of llamas with no abnormalities of the external ear or surrounding tissues. For each of 10 llamas, the head was separated from the neck at the level of the atlantoaxial joint before the head was scanned and dissected. The white-edged boxes in panels A, B, and C indicate the location of higher-magnification images that were used to perform measurements of the osseous external acoustic meatus, tympanic cavity, and tympanic bulla, respectively. Free gas around the brain is secondary to the method of euthanasia used (captive bolt technique). R = Right side. L = Left side.
Citation: American Journal of Veterinary Research 73, 1; 10.2460/ajvr.73.1.42
To compare the size of the llama heads, measurements of length and height of each skull were obtained. The length of a head was obtained by measuring the distance from the rostral border of the incisive bone to the external occipital protuberance on sagittal CT images at the level of the nasal septum. The height of a head was obtained by measuring the distance from the dorsal internal cortex of the skull, at the level of the sagittal crest, to the internal cortex of the base of the basisphenoid on a transverse CT image at the level of the osseous external acoustic meatus. When fractures of the external or middle ear attributable to application of the captive bolt were observed, these areas were excluded from the measurements.
The measurements of the osseous external acoustic meatus were performed on a transverse CT image in which the external ear canal was visible at its maximum length and width. Seven measurements of the osseous external acoustic meatus (designated as OEAM 1 through 7) were obtained. The length (OEAM 1) was measured along a line following the dorsal margin of the osseous external acoustic meatus from the porus to the dorsal aspect of the tympanic annulus of the tympanic membrane. The dorsoventral angle (OEAM 2) was measured as the ventral angle between a straight line traced from the dorsal aspect of the external acoustic meatus porus to the middle point of OEAM 1 and a straight line traced from the middle point of OEAM 1 to the dorsal aspect of the tympanic annulus. The lateral-vertical diameter (OEAM 3) was measured as a vertical line from the dorsal to ventral border of the osseous external acoustic meatus porus, oriented in a 90° angle from the dorsal wall of the meatus. The intermediate diameter (OEAM 4) was measured as a line traced from the dorsal wall to the ventral wall of the osseous external acoustic meatus, oriented in a 90° angle from the dorsal wall at the halfway point along OEAM 1. The medial diameter (OEAM 5) was measured as a line traced from the dorsal wall to the ventral wall of the osseous external acoustic meatus, oriented at an angle of 90° from the dorsal wall at the level of the tympanic annulus of the tympanic membrane. The horizontal-rostrocaudal diameter (OEAM 6) was measured as the horizontal diameter of the osseous external acoustic meatus porus. The horizontal-medial diameter (OEAM 7) was measured as the horizontal diameter of the osseous external acoustic meatus at the level of the tympanic annulus.
The tympanic cavity assessments were performed on a transverse CT image in which the head of the malleus was visible and on a dorsal image in which the widest opening of the auditory tube was identified. The caudolateral and caudomedial processes as well as the stylohyoid fossa of the tympanic bulla were measured on a transverse CT image in which the external ear canal was visible at its maximum length. Three measurements of the tympanic cavity (designated as TC1 through 3) were obtained. The oblique dorsoventral height (TC1) was measured as a line traced from the epitympanic recess to the floor of the tympanic cavity. The mediolateral width (TC2) was measured as a line traced from the promontory to the dorsal aspect of the tympanic annulus of the tympanic membrane. The rostrocaudal length (TC3) was measured as a line traced from the rostral wall (paries caroticus) to the caudal wall (paries mastoideus) of the tympanic cavity at the level of the widest opening of the auditory tube.
The body of the tympanic bulla was measured in 2 transverse images. One image was obtained immediately rostral to the stylohyoid fossa at the level of the condylar process, and the other was obtained at the level of the neck of the mandible, which is the part that supports the mandibular condyle. Twelve measurements of the tympanic bulla (designated as CLp 1 through 3, CMp 1 through 3, SF 1 and 2, and B 1 through 4) were obtained. The dorsoventral height of the caudolateral process of the tympanic bulla (CLp 1) was measured as a line traced from the ventral border of the osseous external acoustic meatus porus to the most distal edge of the caudolateral process of the tympanic bulla. The proximal mediolateral width of the caudolateral process of the tympanic bulla (CLp 2) was measured as a horizontal line traced from the top of the stylohyoid fossa to the lateral edge of the external cortex of the caudolateral process of the tympanic bulla at the level of the maximum depth of the stylohyoid fossa. The distal mediolateral width of the caudolateral process of the tympanic bulla (CLp 3) was measured as a line traced from the medial edge of the caudolateral process of the tympanic bulla to the lateral edge of the caudolateral process of the tympanic bulla at the level of the tympanohyoid cartilage and stylohyoid joint. The dorsoventral height of the caudomedial process of the tympanic bulla (CMp 1) was measured as a line traced from the floor of the tympanic cavity to the distal edge of the caudomedial process of the tympanic bulla at the level of the osseous external acoustic meatus. The proximal mediolateral width of the caudomedial process of the tympanic bulla (CMp 2) was measured as a line traced from the medial edge of the caudomedial process of the tympanic bulla cortex of the petrous portion of the temporal bone to the top of the stylohyoid fossa. The distal mediolateral width of the caudomedial process of the tympanic bulla (CMp 3) was measured as a line traced from the medial edge of the caudomedial process of the tympanic bulla at the level of the joint between the basisphenoid and caudomedial process of the tympanic bulla to the lateral edge of the caudomedial process of the tympanic bulla. Dorsoventral height of the stylohyoid fossa (SF 1) was measured as a line traced from the top of the stylohyoid fossa to the most ventral edges of caudolateral and caudomedial processes of the tympanic bulla. The mediolateral diameter of the lumen of the stylohyoid fossa (SF 2) was measured as a horizontal line traced at the level of the tympanohyoid cartilage and stylohyoid joint. The caudoproximal width of the tympanic bulla (B 1) was measured as a line traced from the medial edge of the body limit of the petrous portion of the temporal bone to the lateral edge of the body. The caudodistal width of the tympanic bulla (B 2) was measured as a line traced rostral to the stylohyoid fossa and meatus from the medial edge of the tympanic bulla at the ventral edge of the basisphenoid to the lateral edge of the tympanic bulla. The intermediate width of the tympanic bulla (B 3) was measured as a line traced caudal to the temporo-mandibular joint from the medial edge of the body at the ventral edge of the basisphenoid to the lateral edge of the tympanic bulla. The rostral width of the tympanic bulla (B 4) was measured as a line traced caudal to the neck of the mandible from the medial edge of the body at the ventral edge of the presphenoid to the lateral edge of the tympanic bulla. Additionally, the caudorostral length of the tympanic bulla (CRL) was measured as a line traced from the lateral border of the caudolateral process of the tympanic bulla toward the apex of the tympanic bulla at the level of the ventral edge of the occipital condyle. The caudorostral angle of the tympanic bulla (CR) was measured as the lateral rostral angle formed by the intersection of a line traced between the caudal border of the mandible and the paracondylar process and a second line traced from the most lateral extent of the caudolateral process to the apex of the tympanic bulla.
Statistical analysis—After the data were tested for normality by use of the Kolmogorov-Smirnoff test, data for each measurement were compared between the right and left ear by use of a paired t test. Because no differences between right and left ears were found, the means of the left and right ear measurements for each head were used for all subsequent analyses. For males and females, the mean, SD, and 95% CI were calculated for each measurement of interest. Data for each measurement were compared between sexes by use of the independent t test. All analyses were performed by use of a commercial software package.c For all comparisons, a value of P < 0.05 was used to determine significance.
Results
For the measurements of interest, there were no significant differences between the right and left sides of the head. For males, mean ± SD head length was 31.0 ± 0.7 cm (95% CI, 30.46 to 31.57 cm); for females, mean head length was 30.7 ± 0.8 cm (95% CI, 29.86 to 31.49 cm). For males, mean head height was 7.5 ± 0.3 cm (95% CI, 7.31 to 7.75 cm); for females, mean head height was 7.4 ± 0.3 cm (95% CI, 6.72 to 8.08 cm). The length or height of llama heads did not differ between sexes (all P ≥ 0.05).
Osseous external acoustic meatus—The osseous external acoustic meatus was part of the tympanic division of the temporal bone with a clear demarcation from the mastoid process of the petrous division of the temporal bone, which was caudally situated (Figure 2). The osseous external acoustic meatus was located caudal to the zygomatic process of the temporal bone. The osseous external acoustic meatus was surrounded by bony structures containing small air-filled cells. These air compartments were most numerous on the ventral aspect toward the tympanic bulla. The widest diameter of the osseous external acoustic meatus was located laterally at the level of the joint with the cartilaginous portion of the canal. The narrowest portion of the osseous external acoustic meatus was located medially at the level of the tympanic annulus. The osseous external acoustic meatus curved ventrally as it coursed medially. The osseous external acoustic meatus was significantly (P < 0.05) longer in males (mean ± SD, 2.5 ± 0.2 cm) than in females (2.4 ± 0.2 cm; Table 1). The mean caudorostral angle was significantly (P < 0.05) smaller in males (113 ± 3.1°) than in females (120 ± 4.1°). The overall mean angle ± SD for females and males was 144 ± 9.7°. The measurements of the osseous external acoustic meatus of 1 side of the head of 1 female llama could not be obtained, as part of the meatus was damaged because the euthanasia technique involved use of a captive bolt.
Representative transverse (A and B), dorsal (C), and sagittal (D) CT images of the right osseous external acoustic meatus of the disarticulated head of an adult llama. A—Measurement of the length of the osseous external acoustic meatus (OEAM 1) is illustrated by the dashed line, and measurement of the dorsoventral angle of the osseous external acoustic meatus (OEAM 2) is illustrated by the solid line. B—Measurements of the lateral vertical diameter (OEAM 3), the intermediate diameter (OEAM 4), and medial diameter (OEAM 5) of the osseous external acoustic meatus are illustrated by dashed lines (α = 90°). C—Measurement of the horizontal rostrocaudal diameter of the osseous external acoustic meatus (OEAM 6) is illustrated by the dashed line. D—Measurement of the horizontal medial diameter (OEAM 7) of the osseous external acoustic meatus is illustrated by the dashed line. Free gas around the brain is secondary to the method of euthanasia used (captive bolt technique). R = Right side. L = Left side.
Citation: American Journal of Veterinary Research 73, 1; 10.2460/ajvr.73.1.42
Measurements of the osseous external acoustic meatus obtained from CT images of the disarticulated heads of 10 llamas without abnormalities of the external ear or associated soft tissues.
| CT image | Measurement | Male(n = 6) | Female (n = 4) |
|---|---|---|---|
| Transverse | OEAM 1 (cm) | 2.5 ± 0.2 (2.42–2.66) | 2.4 ± 0.2 (2.26–2.63) |
| OEAM 2 (°) | 147.2 ± 9.3 (141.3–153.1) | 137.9 ± 8.0 (130.4–145.3) | |
| OEAM 3 (cm) | 0.5 ± 0.1 (0.43–0.54) | 0.5 ± 0.1 (0.38–0.53) | |
| OEAM 4 (cm) | 0.4 ± 0.1 (0.37–0.46) | 0.5 ± 0.1 (0.36–0.59) | |
| OEAM 5 (cm) | 0.3 ± 0.1 (0.26–0.34) | 0.3 ± 0.2 (0.18–0.33) | |
| Dorsal | OEAM ± (cm) | 0.7 ± 0.2 (0.58–0.79) | 0.6 ± 0.1 (0.55–0.65) |
| Sagittal | OEAM 7 (cm) | 0.7 ± 0.1 (0.58–0.74) | 0.6 ± 0.1 (0.47–0.67) |
Data are reported as mean ± SD (95% CI). Measurements could not be performed in 1 ear of 1 female llama because the area was damaged during euthanasia (captive bolt technique). Measurements of interest were as follows: OEAM 1 = Length (measurement along a line following the dorsal margin of the osseous external acoustic meatus from the porus to the dorsal aspect of the tympanic annulus of the tympanic membrane). OEAM 2 = Dorsoventral angle (ventral angle between a straight line traced from the dorsal aspect of the external acoustic meatus porus to the midpoint of OEAM 1 and a straight line traced from the midpoint of OEAM 1 to the dorsal aspect of the tympanic annulus). OEAM 3 = Lateral-vertical diameter (measurement along a vertical line from the dorsal to ventral border of the OEAM porus, oriented in a 90° angle from the dorsal wall of the meatus). OEAM 4= Intermediate diameter (measurement along a line traced from the dorsal to the ventral wall of the OEAM, oriented in a 90° angle from the dorsal wall at the midpoint of OEAM 1). OEAM 5 = Medial diameter (measurement along a line traced from the dorsal to the ventral wall of the osseous external acoustic meatus, oriented at an angle of 90° from the dorsal wall at the level of the tympanic annulus of the tympanic membrane). OEAM 6 = Horizontal-rostrocaudal diameter (horizontal diameter of the osseous external acoustic meatus porus). OEAM 7 = Horizontal-medial diameter (horizontal diameter of the osseous external acoustic meatus at the level of the tympanic annulus).
Tympanic cavity—The tympanic cavity in llamas was a lateromedially flattened cavity with an oblique axis in a dorsolateral to ventromedial orientation (Figure 3; Table 2). The largest dimension of the tympanic cavity was the rostrocaudal length, followed by the oblique dorsoventral height and then the mediolateral width. The tympanic cavity walls, structures, and spaces (eg, the epitympanic recess, malleus, promontorius, auditory tube, and the communication area with the tympanic bulla in the ventral wall) were clearly identified. The tympanic membrane was identified in both ears in 6 heads by use of transverse images. In 4 heads, the tympanic membrane could be identified on only 1 side. Changing from a bone window to a soft tissue window or performing additional reconstructed views did not improve the visualization of the tympanic membrane.
Representative transverse (A) and dorsal (B) CT images of the right tympanic cavity at the level of the head of the malleus (HM) in the disarticulated head of an adult llama. A—Measurement of the oblique dorsoventral height (TC 1) and the mediolateral width (TC 2) are illustrated. B—Measurement of the rostrocaudal length (TC 3) of the tympanic cavity at the level of the maximum medial opening of the auditory tube (AT) is illustrated. Free gas around the brain is secondary to the method of euthanasia used (captive bolt technique).
Citation: American Journal of Veterinary Research 73, 1; 10.2460/ajvr.73.1.42
Measurements of the tympanic cavity obtained from CT images of the disarticulated heads of 10 llamas without abnormalities of the external ear or associated soft tissues.
| CT image | Measurement | Male(n = 6) | Female (n = 4) |
|---|---|---|---|
| Transverse | TC 1 (cm) | 1.3 ± 0.0 (1.29–1.35) | 1.3 ± 0.1 (1.28–1.48) |
| TC 2 (cm) | 0.5 ± 0.1 (0.46–0.58) | 0.6 ± 0.0 (0.52–0.64) | |
| Dorsal | TC 3 (cm) | 1.4 ± 0.1 (1.67–1.49) | 1.4 ± 0.1 (1.30–1.46) |
Data are reported as mean ± SD (95% CI). Measurements could not be performed in 1 ear of 1 female llama because the area was damaged during euthanasia (captive bolt technique). Measurements of interest were as follows: TC 1 = Oblique dorsoventral height (measured along a line traced from the epitympanic recess to the floor of the tympanic cavity). TC 2 = Mediolateral width (measured along a line traced from the promontory to the dorsal aspect of the tympanic annulus of the tympanic membrane). TC 3= Rostrocaudal length (measured along a line traced from the rostral wall [paries caroticus] to the caudal wall [paries mastoideus] of the tympanic cavity at the level of the widest opening of the auditory tube).
Tympanic bulla—For the morphometric study of the complex structure of the tympanic bulla, this region was divided into a caudolateral and caudomedial process, body, and apex (Figure 4; Tables 3 and 4). The caudal bony projections of the tympanic bulla were separated by the stylohyoid fossa into a larger caudolateral and smaller caudomedial process. The dorsal half of the fossa was occupied by the tympanohyoid cartilage and the ventral half by the stylohyoid bone. The joint between these structures was located inside the fossa. The body was a bulbous portion of the tympanic bulla situated rostrally to an imaginary line traced from the rostral border of the caudolateral process of the tympanic bulla along the rostral edge of the stylohyoid fossa. The pyramidal shape of the body was situated in such a way that the base was facing the caudal processes and the apex was rostrally directed (Figures 5–7). The apex corresponded to the muscular process of the tympanic portion of the temporal bone and represented the rostral aspect of the body. The entire tympanic bulla contained a honeycombed, bony structure with air-filled cells.
Representative transverse CT images of the right tympanic bulla of the disarticulated head of an adult llama. A—Measurements of the dorsoventral height of the caudolateral process of the tympanic bulla (CLp 1), proximal mediolateral width of the caudolateral process of the tympanic bulla (CLp 2), distal mediolateral width of the caudolateral process of the tympanic bulla (CLp 3) of the caudolateral process of the tympanic bulla, dorsoventral height of the caudomedial process of the tympanic bulla (CMp 1), proximal mediolateral width of the caudomedial process of the tympanic bulla (CMp 2), and distal mediolateral width of the caudomedial process of the tympanic bulla (CMp 3) are illustrated by lines in the image. B—Measurements of the dorsoventral height (SF 1) and the mediolateral diameter of the lumen (SF 2) of the stylohyoid fossa are illustrated by lines in the image. Free gas around the brain is secondary to the method of euthanasia used (captive bolt technique).
Citation: American Journal of Veterinary Research 73, 1; 10.2460/ajvr.73.1.42
Representative photographs of the ventral (A) and left lateral (B) views of the disarticulated skull of an adult llama illustrating the location, shape, and parts of the left tympanic bulla. The dashed line in panel A represents the imaginary line between the caudal processes and body of the tympanic bulla.
Citation: American Journal of Veterinary Research 73, 1; 10.2460/ajvr.73.1.42
Representative transverse CT images of the right tympanic bulla of the disarticulated head of an adult llama. A—Measurements of the caudoproximal width of the tympanic bulla (B 1) and caudodistal width of the tympanic bulla (B 2) immediately rostral to the stylohyoid fossa are illustrated by lines in the image. B—Measurement of the intermediate width of the tympanic bulla (B 3) at the level of the caudal border of the condylar process of the mandible (CP) is illustrated by a line in the image. C—Measurement of the rostral width of the tympanic bulla (B 4) at the level of the caudal border of the neck of the mandible (NM) is illustrated by a line in the image. Free gas around the brain is secondary to the method of euthanasia used (captive bolt technique).
Citation: American Journal of Veterinary Research 73, 1; 10.2460/ajvr.73.1.42
Representative dorsal CT image of the right tympanic bulla of the disarticulated head of an adult llama. Measurement of the caudorostral length (CRL) is illustrated by the dashed line. Measurement (α) of the caudorostral angle (CRA) of the caudolateral process and body of the tympanic bulla at the level of the ventral border of the occipital condyle is also illustrated. The CRA is formed by the intersection of a line traced between the caudal border of the neck of the mandible (NM) and the paracondylar process (PP) and a second line traced from the most lateral extent of the caudolateral process (CLp) to the apex (A) of the tympanic bulla. B = Body of the tympanic bulla. CMp = Caudomedial process. SF = Stylohyoid fossa.
Citation: American Journal of Veterinary Research 73, 1; 10.2460/ajvr.73.1.42
Measurements of the tympanic bulla obtained from CT images of the disarticulated heads of 10 llamas without abnormalities of the external ear or associated soft tissues.
| CT image | Measurement | Male(n = 6) | Female (n = 4) |
|---|---|---|---|
| Transverse | CLp 1 (cm) | 4.3 ± 0.3 (4.18–4.50) | 4.5 ± 0.3 (4.26–4.80) |
| CLp 2 (cm) | 2.0 ± 0.2 (1.87–2.08) | 1.9 ± 0.3 (1.60–2.15) | |
| CLp 3 (cm) | 1.4 ± 0.2 (1.31–1.56) | 1.3 ± 0.3 (1.00–1.57) | |
| CMp 1 (cm) | 2.2 ± 0.2 (2.07–2.31) | 2.3 ± 0.3 (2.02–2.56) | |
| CMp 2 (cm) | 1.3 ± 0.2 (1.15–1.39) | 1.1 ± 0.1 (0.98–1.22) | |
| CMp 3 (cm) | 1.1 ± 0.4 (0.84–1.31) | 0.9 ± 0.3 (0.67–1.19) | |
| SF 1 (cm) | 2.1 ± 0.2 (1.93–2.24) | 2.3 ± 0.2 (2.15–2.45) | |
| SF 2 (cm) | 0.5 ± 0.1 (0.49–0.56) | 0.5 ± 0.1 (0.42–0.55) | |
| B 1 (cm) | 2.3 ± 0.8 (1.78–2.89) | 2.7 ± 0.8 (1.88–3.49) | |
| B 2 (cm) | 2.6 ± 0.4 (2.3–2.83) | 2.6 ± 0.4 (2.27–3.00) | |
| B 3 (cm) | 2.0 ± 0.2 (1.84–2.15) | 2.1 ± 0.1 (1.99–2.24) | |
| B 4 (cm) | 1.2 ± 0.4 (0.99–1.43) | 1.6 ± 0.3 (1.26–1.94) |
Data are reported as mean ± SD (95% CI). Measurements could not be performed in 1 ear of 1 female llama because the area was damaged during euthanasia (captive bolt technique). Measurements of interest were as follows: CLp 1 = Dorsoventral height of the caudolateral process of the tympanic bulla (measured along a line traced from the ventral border of the osseous external acoustic meatus porus to the most distal edge of the caudolateral process of the tympanic bulla). CLp 2 = Proximal mediolateral width of the caudolateral process of the tympanic bulla (measured along a horizontal line traced from the top of the stylohyoid fossa to the lateral edge of the caudolateral process of the tympanic bulla external cortex at the level of the maximum depth of the stylohyoid fossa). CLp 3 = Distal mediolateral width of the caudolateral process of the tympanic bulla (measured along a line traced from the medial edge of the caudolateral process of the tympanic bulla to the lateral edge of the caudolateral process of the tympanic bulla at the level of the tympanohyoid cartilage and stylohyoid joint). CMp 1 = Dorsoventral height of the caudomedial process of the tympanic bulla (measured along a line traced from the floor of the tympanic cavity to the distal edge of the caudomedial process of the tympanic bulla at the level of the osseous external acoustic meatus). CMp 2 = Proximal mediolateral width of the caudomedial process of thetympanic bulla (measured along a line traced from the medial edge of the caudomedial process of the tympanic bulla cortex of the petrous portion of the temporal bone to the top of the stylohyoid fossa). CMp 3= Distal mediolateral width of the caudomedial process of the tympanic bulla (measured along a line traced from the medial edge of the caudomedial process of the tympanic bulla at the level of the joint between the basisphenoid and caudomedial process of the tympanic bulla to the lateral edge of the caudomedial process of the tympanic bulla). SF1 = Dorsoventral height of the stylohyoid fossa (measured along a line traced from the top of the stylohyoid fossa to the mostventral edges of the caudolateral and caudomedial processes of the tympanic bulla). SF 2 = Mediolateral diameter of the stylohyoid fossa lumen (measured along a horizontal line traced at the level of the tympanohyoid cartilage and stylohyoid joint). B 1 = Caudoproximal width of the tympanic bulla (measured along a line traced from the medial edge of the body limit of the petrous portion of the temporal bone to the lateral edge of the body). B 2 = Caudodistal width of the tympanic bulla (measured along a line traced rostral to the stylohyoid fossa and meatus from the medial edge of the body at the ventral edge of the basisphenoid to the lateral edge of the body). B 3= Intermediate width of the tympanic bulla (measured along a line traced caudal to the tem poromandibular joint from the medial edge of the body at the ventral edge of the basisphenoid to the lateral edge of the body). B 4= Rostral width of the tympanic bulla (measured along a line traced caudal to the neck of the mandible from the medial edge of the body at the ventral edge of the presphenoid to the lateral edge of the body).
Measurements of the caudorostral length and caudorostral angle of the caudolateral process and body of the tympanic bulla obtained from CT images of the disarticulated heads of 10 llamas without abnormalities of the external ear or associated soft tissues.
| CT image | Measurement | Male(n = 6) | Female (n = 4) |
|---|---|---|---|
| Dorsal | CRL (mm) | 3.4 ± 0.3 (3.24–3.60) | 3.2 ± 0.2 (3.08–3.34) |
| CRA (°) | 112.8 ± 3.1 (110.9–114.8) | 119.8 ± 4.1 (116.4–123.1) |
Data are reported as mean ± SD (95% CI). Measurements could not be performed in 1 ear of 1 female llama because the area was damaged during euthanasia (captive bolt technique). Measurements of interest were as follows: CRL = Caudorostral length of the caudolateral process and body of the tympanic bulla (measured along a line traced from the lateral border of the caudolateral process of the tympanic bulla toward the apex of the tympanic bulla at the level of the ventral edge of the occipital condyle). CRA= Caudorostral angle of the caudolateral process and body of the tympanic bulla (measured as the lateral rostral angle formed by the intersection of a line traced between the caudal border of the mandible and the paracondylar process and a second line traced from the most lateral extent of the caudolateral process to the apex of the tympanic bulla).
Discussion
In the disarticulated llama heads used in the present study, the osseous external acoustic meatus appeared in the CT images as a long, narrow, ventrally curved canal intimately related with the tympanic bulla. The bend occurred approximately halfway between the porus and the tympanic annulus, with an overall mean ± SD angle for females and males of 144 ± 9.7°. A previous report2 described the osseous external acoustic meatus in adult South American camelids as a canal, which bent ventrally at a depth of 1.8 cm, forming an angle of 120°; however, it was not clear at which anatomic location those measurements were obtained. The location of the osseous external acoustic meatus as part of the tympanic division of the temporal bone was similar to that described for other domestic animals12 but did not agree with results of a previous study in llamas,2 which indicated that the osseous ear canal appeared to enter the petrous division of the temporal bone immediately ventral to the zygomatic process. The external ear canal lumen was ovoid, with an overall external vertical diameter of 0.5 ± 0.1 cm and horizontal diameter of 0.6 ± 0.1 cm in males and females; the canal narrowed in vertical diameter as it coursed internally. This is in agreement with findings of a previous study1 performed in an alpaca. In another study13 of a skeletal preparation of 1 large male llama, the osseous external meatus orifice was 6 mm in diameter and narrowed to 4 mm at the bend. The lack of detail regarding the anatomic location where the measurements were obtained in that study makes it difficult to compare those data with the CT data obtained in the present study. However, the descriptive information and measurements obtained in the present study form a basis for comparison with camelids with abnormalities, such as congenital or acquired disease of the osseous external acoustic meatus.
The tympanic cavity in llamas was contained within the petrous and tympanic portions of the temporal bone, as described for other domestic animals.12–15 Because the tympanic bulla did not have a fundic cavity, it was measured as a separate structure in the study of this report. The tympanic cavity appeared as a lateromedially flattened cavity with an oblique axis in a dorsolateral to ventromedial orientation. The lengths of 15 mm described for the tympanic cavity in humans3 and 13.3 mm in sheep3 were similar to the tympanic cavity length of 1.4 ± 0.1 cm observed in our study. The mean height of the human tympanic cavity has been described as 15 mm,3 similar to the overall height of 1.3 ± 0.1 cm in female and male llamas. In sheep, the mean height of the tympanic cavity is 18.9 mm,3 but that measurement includes the tympanic bulla.
The epitympanic recess and the atrium of the tympanic cavity in the llama heads examined in the present study retained the general shape of those structures in other domestic animals.13 The malleus was observed without difficulties. The head of the malleus extended into the epitympanic recess, whereas the neck and the manubrium were in the atrium of the tympanic cavity. The tympanic opening of the auditory tube was located rostrally in the middle wall of the tympanic cavity. The promontory, which is the prominence of the cochlea into the tympanic cavity, was observed in the medial wall of the tympanic cavity; its CT characteristics were similar to findings in dogs6 and sheep.3
The tympanic bulla of the llama heads was a bony structure and was considerably different from the bullae of many other domestic animals. Dogs, cats, and sheep have spherical bullae with a single fundic cavity.3,12–16 In contrast, llamas had conical, multicompartmental tympanic bullae with air-filled cells surrounded by bony trabeculae. These anatomic features have been reported previously for llamas2,17 and alpacas.1,d The camelid bulla is also similar in shape to that of the dromedary camel.4 In sagittal CT views in the present study, the bulla appeared quadrilateral and located caudomedial to the neck of the mandible; in dorsal CT views, it appeared pyramidal. It had a small caudomedial process closely related with the paracondylar process of the occipital bone, a large caudolateral process connected to the osseous external acoustic meatus, a body, and an apex. Results of a previous studyd indicated that the entire bulla was draped over the proximal portions of the stylohyoid bone, creating the stylohyoid fossa in alpacas. That was not the case in llamas, in which only the proximal third of the stylohyoid bone was completely enveloped by the tympanic bulla. The distal two-thirds of the stylohyoid fossa were incompletely covered by the tympanic bulla, leaving a caudal aperture of the fossa.
The honeycombed interior of the tympanic bulla in the llama heads had some structural similarity to the mastoid process in humans.18 In humans, infections of the middle ear can extend into the bony cells of the mastoid process, thereby complicating treatment. Persistence of infection with mastoiditis may require surgical osteotomy, lavage, and curettage of the infected bone.18–20 A similar surgical treatment was attempted in an alpaca without success.14 Greater understanding of the shape and complexity of the camelid tympanic bulla may facilitate future treatment efforts.
In the present study, the head size in male and female llamas did not differ significantly. The lack of detectable difference in head size may be attributable to the small number of animals included in the study. However, there were differences in the length of the osseous external acoustic meatus, which was slightly longer in males than in females, and in the caudorostral angle of the tympanic bulla, which was smaller in males than in females. Overall, the osseous external acoustic meatus was a long and narrow canal with a curvature that bent ventrally. The 2 dorsal areas of the tympanic cavity (epitympanic recess and atrium) were similar in shape to that of the same chambers in sheep. The ventral portion of the tympanic cavity or tympanic bulla in llamas differed in appearance from those of dogs, cats, and sheep. The tympanic bulla was a pneumatized bone with multiple compartments filled with air and connected with the atrium of the tympanic cavity. The present study has provided new information about the shape, size, and location of the osseous external acoustic meatus, tympanic cavity, and tympanic bulla in adult llamas without ear disease.
ABBREVIATIONS
| CI | Confidence interval |
| CT | Computed tomography |
Toshiba Aquilion, Toshiba America Medical Systems Inc, Tustin, Calif.
eFilm, version 3.3.0, Merge Healthcare, Heartland, Wis.
GraphPad Prism, version 5.01, GraphPad Software Inc, La Jolla, Calif.
Silver TI. Computed tomographic evaluation of otitis in the alpaca (abstr), in Proceedings. Am Coll Vet Intern Med Forum Can Vet Med Assoc Conv 2009;262–264.
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