Computed tomographic examination of the articular process joints of the cervical spine in warmblood horses: 86 cases (2015–2017)

Tibor Rovel From the Department of Veterinary Medical Imaging, Biometrics Research Group,

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Marieke Zimmerman Equitom Equine Hospital, 3560 Meldert, Belgium.

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Luc Duchateau From the Department of Veterinary Medical Imaging, Biometrics Research Group,

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Catherine Delesalle Department of Virology, Parasitology and Immunology, Research Group Comparative Physiology, Faculty of Veterinary Medicine, Ghent University, 9820 Merelbeke, Belgium;

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Edouard Adriaensen Equitom Equine Hospital, 3560 Meldert, Belgium.

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Tom Mariën Equitom Equine Hospital, 3560 Meldert, Belgium.

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Jimmy H. Saunders From the Department of Veterinary Medical Imaging, Biometrics Research Group,

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Katrien Vanderperren From the Department of Veterinary Medical Imaging, Biometrics Research Group,

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Abstract

OBJECTIVE

To describe articular process joints (APJs) of the cervical spine in horses on the basis of CT and to determine whether abnormalities were associated with clinical signs.

ANIMALS

86 client-owned warmblood horses.

PROCEDURES

Horses that underwent CT of the cervical spine between January 2015 and January 2017 were eligible for study inclusion. Medical records were reviewed for age, body weight, breed, sex, history, clinical signs, and CT findings. Horses were divided into 3 case groups and 1 control group on the basis of clinical signs.

RESULTS

70 warmblood horses were cases, and 16 were controls. Abnormalities were more frequent from C5 through T1 and were severe in only horses from the case group. Narrowing of the intervertebral foramen was common in horses in the case group (85.7%), often owing to enlarged, misshaped articular processes, followed by degenerative changes, periarticular osteolysis, cyst-like lesions, and fragmentation. High articular process-to-vertebral body (C6) ratio (APBR) and high-grade narrowing of the intervertebral foramen and periarticular osteolysis were noted for horses with forelimb lameness or signs of cervical pain or stiffness. No association was identified between APBR and age or sex. An APBR > 1.5 was found in only horses in the case group, and 32.3% of APJs with APBRs > 1.5 did not have any degenerative changes and periarticular osteolysis.

CONCLUSIONS AND CLINICAL RELEVANCE

CT was useful to identify abnormalities of the APJs of the cervical spine. An association existed between CT findings and clinical signs. The APJs can be enlarged without concurrent degenerative changes.

Abstract

OBJECTIVE

To describe articular process joints (APJs) of the cervical spine in horses on the basis of CT and to determine whether abnormalities were associated with clinical signs.

ANIMALS

86 client-owned warmblood horses.

PROCEDURES

Horses that underwent CT of the cervical spine between January 2015 and January 2017 were eligible for study inclusion. Medical records were reviewed for age, body weight, breed, sex, history, clinical signs, and CT findings. Horses were divided into 3 case groups and 1 control group on the basis of clinical signs.

RESULTS

70 warmblood horses were cases, and 16 were controls. Abnormalities were more frequent from C5 through T1 and were severe in only horses from the case group. Narrowing of the intervertebral foramen was common in horses in the case group (85.7%), often owing to enlarged, misshaped articular processes, followed by degenerative changes, periarticular osteolysis, cyst-like lesions, and fragmentation. High articular process-to-vertebral body (C6) ratio (APBR) and high-grade narrowing of the intervertebral foramen and periarticular osteolysis were noted for horses with forelimb lameness or signs of cervical pain or stiffness. No association was identified between APBR and age or sex. An APBR > 1.5 was found in only horses in the case group, and 32.3% of APJs with APBRs > 1.5 did not have any degenerative changes and periarticular osteolysis.

CONCLUSIONS AND CLINICAL RELEVANCE

CT was useful to identify abnormalities of the APJs of the cervical spine. An association existed between CT findings and clinical signs. The APJs can be enlarged without concurrent degenerative changes.

Introduction

Pathologic changes of the cervical spine in horses are causes of poor performance, ataxia, forelimb lameness, and cervical pain and stiffness.1,2,3 Radiology and ultrasonography of the cervical region are routinely performed,1,4,5 and scintigraphy can reveal information about bone metabolism.2,4 However, these imaging modalities have several limitations that prevent complete evaluation of the cervical region, and CT and MRI may overcome these limitations.2,6,7,8,9,10,11,12

Information about the CT features of the equine cervical articular process joint (APJ) is scant. The anatomy of the APJ capsule and outpouches for 6 normal adult horses have been assessed post mortem with CT.13 Ex vivo CT and MRI findings were compared with gross anatomical sections in 3 horses,12 and the normal anatomy in 2 foals from the occipital condyles to C7 was determined via 3-D CT.14 The clinical use of CT for the evaluation of suspected cervical pathologic changes has been described in only 2 reports, 1 of which was a case report.15,16 Computed tomography and MRI of horses had been limited because CT and MRI machines have been unable to accommodate a horse. Given recent advancements, however, CT is now possible and is being used for diagnostic purposes at equine specialty hospitals.

The objectives of the retrospective study reported here were to describe the antemortem CT findings of diseased APJs of the cervical spine of horses and to investigate whether CT findings were associated with clinical signs. Computed tomography was expected to be a useful modality to identify lesions of the APJs of the cervical spine, and an association was expected between CT findings and clinical signs.

Materials and Methods

Animals

All horses that underwent CT of the cervical spine between January 2015 and January 2017 were included in the study. Medical records were reviewed, and collected data were age, body weight, breed, sex, history, clinical signs, and diagnostic imaging findings. Horses were divided into case and control groups.

Horses were assigned to the control group (group 1) if they had a normal locomotor examination and no history of locomotion problems or had lameness that resolved following nonaxial diagnostic analgesia (peripheral nerve block or intrasynovial analgesia performed at the level of or distal to the shoulder) and did not show any signs of ataxia or cervical pain or stiffness during the examination. Computed tomography of the cervical spine was performed at the request of the referring veterinarian or the horse owner.

Horses were assigned to the case group if they had clinical signs that indicated lesion neurolocalization in the cervical spine, forelimb lameness that failed to improve following a nonaxial diagnostic analgesia, or signs of cervical pain or stiffness (discomfort with palpation or reduced range of motion of the cervical region, or blocking with the neck in a ventral position). Case horses were subdivided into 3 groups according to their primary clinical sign: group 2, horses with ataxia; group 3, horses with forelimb lameness that failed to resolve following nonaxial diagnostic analgesia; or group 4, horses with signs of cervical pain or stiffness.

CT image acquisition

Horses were anesthetized and positioned in right lateral recumbency for image acquisition with a standard-bore (diameter, 72 cm), 4-slice, third-generation CT machine that used helical acquisition and the following scanning parameters: 135 kVp, 200 mA, collimator pitch of 1.1, detector pitch of 4.5, 1-mm slice thickness, 1-mm reconstruction interval, matrix size of 512 × 512 pixels, and field of view of 400 mm. A bone or soft tissue reconstruction filter was applied, and images were acquired from the occiput to T1. Two scans were necessary to image the entire cervical spine: one from the occiput through C3 and another from C3 through T1.

CT image interpretation

Computed tomographic images were analyzed retrospectively on a dedicated workstation with a DICOM viewer (Osirix; Pixmeo SARL). Images were evaluated in bone (level, 500 HU; width, 1,500 HU) and soft tissue (level, 250 HU; width, 650 HU) windows. Two-dimensional transverse, sagittal, and dorsal planar images were made by use of multiplanar reconstruction. A board-certified equine radiologist (TR) who was blinded to patient history, physical examination findings, and any prior reports reviewed all images. The report generated at the time of CT by a second investigator (MZ) who was not blinded to patient history and physical examination findings and was experienced in interpreting CT images of the equine cervical spine was also considered in the analysis. Images were reviewed for the presence of various lesions of the APs (narrowing of the intervertebral foramen [NIF], fragmentation, periarticular osteolysis [bony lysis adjacent to the APJ recesses], degenerative changes [ie, bony proliferation at the joint margin and at the attachment site of the joint capsule, presence of synovial effusion, irregularities of the subchondral bone surface, modification of the signal attenuation of the subchondral bone and adjacent part of the spongious bone, modification of thickness of both the joint space and cartilage layers {assessed from subchondral bone to subchondral bone}], cyst-like lesion, focal ventral bone formation, and dorsal protuberance), and each lesion was graded 0 to 3 on a scale that was adapted from previous studies (Table 1).2,5,7,12,13,14,16,17 The presence of a specific lesion and the final grade for each lesion were determined by consensus of the interpretation by the 2 investigators. A lesion had to be seen in at least 2 planes for it to be considered as a lesion.

Table 1

Grading scheme that was used to describe the presence or severity of various abnormalities of articular process joints (APJs) of the cervical spine identified with CT in 86 client-owned warmblood horses, which included 70 clinical cases and 16 controls.

AP lesion Grade and description
NIF

    Grade 0

  • Normal.

  • Symmetric wide space (minimal distance, > 10 mm) between the ventral aspect of the AP and adjacent vertebral body.

  • Ventral aspect of the AP does not extend ventrally beyond the dorsal margin of the vertebral body.

    Grade 1

  • Mild narrowing of the space between the AP and vertebral body (minimal distance, > 5 mm).

    Grade 2

  • Moderate narrowing (minimal distance, < 5 mm) of the space between the AP and vertebral body, with nearly bone-to-bone contact but without bony changes.

    Grade 3

  • Severe narrowing with bone-to-bone contact between the AP and adjacent vertebral body.

  • Bony changes (sclerosis or lysis) of the adjacent bones with or without modeling of the bony margins at the level of the contact.

Fragmentation

    Grade 0

  • Normal. No fragmentation.

    Grade 1

  • 1 small fragment (longest part of the fragment, < 5 mm).

    Grade 2

  • 1 moderately sized fragment (longest part of the fragment, between 5 and 10 mm) or several small fragments (longest part of each fragment, < 5 mm).

    Grade 3

  • At least 1 large fragment (longest part of the fragment, > 10 mm) or several moderately sized fragments (longest part of each fragment, between 5 and 10 mm).

Periarticular osteolysis

    Grade 0

  • Normal.

  • Regular bony surface of the joint margins and adjacent to the joint recesses, especially at the vertebral pedicle of the cranial vertebra and at the dorsal lamina and spinous process of the caudal vertebra.

    Grade 1

  • 1 small area of a bony defect (depth, < 5 mm).

    Grade 2

  • 1 moderately sized area of a bony defect (depth, between 5 and 10 mm) or several small areas of bony defect (depth, < 5 mm).

    Grade 3

  • At least 1 large area of bony defect (depth, > 10 mm) or several moderately sized areas of bony defects (depth, between 5 and 10 mm).

Degenerative change Mild (grade 1), moderate (grade 2), or severe (grade 3) on the basis of the CT findings of the control group horses and the presence and severity of the following:
  • Bony proliferation at the joint margins and capsule attachment.

  • Synovial effusion.

  • Irregularities of the subchondral bone surface.

  • Modification of the signal attenuation of the subchondral bone, adjacent part of the spongious bone, and thickness of both the joint space and cartilage layers (assessed from subchondral bone to subchondral bone).

  • Joint collapse (recorded as grade 3).

Cyst-like lesion

    Grade 0

  • Normal. No cyst-like lesion.

    Grade 1

  • 1 small cyst-like lesion (diameter, < 5 mm).

    Grade 2

  • 1 moderately sized cyst-like lesion (diameter, between 5 and 10 mm) or several small cyst-like lesions (diameter, < 5 mm).

    Grade 3

  • At least 1 large cyst-like lesion (diameter, > 10 mm) or several moderately sized cyst-like lesions (diameter, between 5 and 10 mm).

Focal ventral bone formation of the AP Presence or absence.
Dorsal protuberance Presence or absence.

NIF = Narrowing of the intervertebral foramen.

To objectively assess the size of the APJs for C2 through T1, the ratio of the cross-sectional area of both the cranial and caudal APs of each vertebra and the maximum cross-sectional area of the cranial aspect of the body of C6 were calculated (Figure 1). Measurements were made in the transverse plane, and multiplanar reconstruction was used to assess the position of the images. Measurements of the cross-sectional area of the cranial and caudal APs were made at the midcraniocaudal one-third of the APJ and perpendicular to the vertebral canal. The maximum cross-sectional area of the cranial aspect of the body of C6 was determined by scrolling through the images of the body of C6 in a craniocaudal direction to visualize the maximum area. The area was subsequently measured cranial to the origin of the pedicles and perpendicular to the vertebral canal. Only 1 vertebral body (C6) was used to calculate these ratios to limit the number of and the time to calculate the measurements and to have a consistent vertebra for reference. The C6 was selected because it is in the middle of the caudal region of the cervical spine. Asymmetry of the joint space was not considered for calculation of the AP-tovertebral body ratio (APBR).

Figure 1
Figure 1

Representative CT images (in bone window), with orientation of the images controlled by use of multiplanar reconstruction, of the C4-C5 articular process joint (APJ; A and B) and C6 vertebra (C) of a warmblood horse of the control group that illustrate the landmarks used to calculate the AP-to-vertebral body ratio. A—Transverse image at the level of the midcraniocaudal aspect of the C4-C5 APJ. Right is at the left of the image. The midcraniocaudal aspect of C4 through C5 was identified by scrolling through the images in a craniocaudal direction. After the image was selected, the closed polygon function of the DICOM viewer (Osirix; Pixmeo SARL) was used to measure the cross-sectional area of the left and right APs. On both sides, the cranial and caudal APs were measured together. B—Transverse image at the level of the maximum cross-sectional area of the cranial aspect of the body of C6. Right is at the left of the image. The maximum cross-sectional area was determined by scrolling through the images in a craniocaudal direction in the area of the body cranial to the origin of the vertebral pedicles to visualize the maximum area. After the image was selected, the closed polygon function of the DICOM viewer was used to measure the cross-sectional area. C—Sagittal image with a purple line that indicates the level of C6 in panel B. The blue line demarcates the dorsal surface of the body of C6, and the purple line is perpendicular to the blue line.

Citation: Journal of the American Veterinary Medical Association 259, 10; 10.2460/javma.20.03.0105

Data analysis

To assess the predictive value of CT findings to distinguish between case (groups 2, 3, and 4) and control (group 1) horses, logistic regression analysis was performed with horse group (either group 2, 3, or 4 vs group 1) as the binary dependent variable and, as the independent variables, the values of the various CT measurements, such as mean or maximum APBR or grade of each abnormality of the APJ (NIF, degenerative changes, periarticular osteolysis, cyst-like lesion, or fragmentation). For groups 2 (ataxia) and 4 (cervical pain or stiffness), analyses were performed with APJ data for C2 through T1. For group 3 (forelimb lameness), analysis was performed with APJ data for only C5 through T1 because the ventral rami of the C6 through T2 spinal nerves innervate the forelimbs.18 The binomial test was used with group 3 data (at the horse level) to assess whether the side of the highest mean or maximum grade of NIF corresponded to the side of the affected (lame) forelimb.

The Spearman rank correlation coefficient test was used to investigate the association between the grade of NIF and the APBR and between the grade of degenerative changes and the presence or absence of focal ventral bone formation. Data for testing were obtained from images acquired at the level of the APJ. To assess the effect of degenerative changes, age, sex, and the affected side (left or right) of the APJ on the APBR, APJ level data were inputted in a mixed model that included horse as a random effect. All statistical analyses were performed with commercially available software (R version 3.6.3; R Foundation). Values of P < 0.05 were considered significant.

Results

Animals

In total, 86 horses had CT of the cervical spine performed during the study period, with 16 horses assigned to the control group (group 1) and 70 assigned to one of the case groups (group 2, n = 23; group 3, 33; or group 4, 14). On the basis of the physical examination, each horse met the criteria for only 1 group, such that each horse was not assigned to > 1 group. All horses were warm-blood horses. For the 16 horses in group 1, 9 were male (geldings, 7; stallions, 2), 7 were female, mean age was 7.4 years (range, 3.0 to 12.3 years), and mean body weight was 553.4 kg (range, 403.5 to 584.9 kg). For the 70 horses in groups 2, 3, and 4, 48 were male (geldings, 38; stallions, 10), 23 were female, mean age was 8.1 years (range, 1.0 to 17.8 years), and mean body weight was 511.2 kg (range, 250.2 to 627.8 kg).

CT findings

The main abnormalities were NIF (n = 214 joints), degenerative changes (190), periarticular osteolysis (70), cyst-like lesions (43), and fragmentation (37; Tables 2 and 3). These abnormalities were more commonly identified from C5 through T1, except for degenerative changes, which were more commonly identified from C3 through C5. Narrowing of the intervertebral foramen, periarticular osteolysis, and cyst-like lesions were most commonly identified for C6 through C7, and fragments were most commonly identified for C7 through T1. The proportions of affected horses and APJs with these abnormalities were higher in the case groups, compared with the control group. The most common identified abnormality for the horses in the case groups was NIF, whereas the most common identified abnormality for the horses in the control group was degenerative changes. Mild (grade 1) to moderate (grade 2) abnormalities were identified in all horses, whereas severe (grade 3) abnormalities were identified in only horses in the case groups.

Table 2

Computed tomographic findings of the APJs of the cervical spine of warmblood horses divided into control (group 1 [n = 16]) and clinical cases (group 2 [23], 3 [33], or 4 [14]).*

CT finding C2 through C3 C3 through C4 C4 through C5 C5 through C6 C6 through C7 C7 through T1 No. of APJs (No. of horses)
NIF
 Group 1 1 0 0 6 11 6 24 (8)
 Group 2 2 1 1 11 30 7 52 (17)
 Group 3 0 0 5 26 50 15 96 (32)
 Group 4 2 0 2 9 18 11 42 (11)
Total 5 1 8 52 109 39 214 (68)
Degenerative change
 Group 1 2 15 6 3 3 0 29 (9)
 Group 2 4 19 14 12 6 0 55 (15)
 Group 3 0 19 21 17 15 5 77 (14)
 Group 4 0 8 6 7 6 2 29 (11)
Total 6 61 47 39 30 7 190 (49)
Periarticular osteolysis
 Group 1 0 0 0 2 3 1 6 (4)
 Group 2 0 1 0 0 14 2 17 (12)
 Group 3 0 0 4 5 22 0 31 (16)
 Group 4 1 0 1 0 12 2 16 (9)
Total 1 1 5 7 51 5 70 (41)
Cyst-like lesions
 Group 1 0 0 0 0 0 3 3 (2)
 Group 2 2 1 4 3 5 4 19 (8)
 Group 3 0 1 0 3 6 2 12 (9)
 Group 4 0 0 0 2 5 2 9 (6)
Total 2 2 4 8 16 11 43 (25)
Fragments
 Group 1 0 0 0 0 1 0 1 (1)
 Group 2 0 2 1 4 2 9 18 (10)
 Group 3 0 1 2 4 0 5 12 (6)
 Group 4 0 0 1 1 0 4 6 (4)
Total 0 3 4 9 3 18 37 (21)

Each horse was assigned to 1 group on the basis of its primary clinical sign. Group 2 horses primarily had ataxia with lesion neurolocalization to the cervical spine, group 3 horses primarily had forelimb lameness that failed to resolve following nonaxial diagnostic analgesia, and group 4 horses primarily had signs of cervical pain or stiffness.

Degenerative changes include bony proliferation at the joint margin and at the attachment site of the joint capsule, presence of synovial effusion, irregularities of the subchondral bone surface, modification of the signal attenuation of the subchondral bone and adjacent part of the spongious bone, and modification of thickness of both the joint space and cartilage layers (assessed from subchondral bone to subchondral bone).

See Table 1 for remainder of key.

Table 3

Computed tomographic findings of the APJs of the cervical spine of the horses of Table 2, with each APJ allocated by horse group* and mean grade of each CT finding or with each horse allocated by horse group and maximum grade of each CT finding.

CT finding No. of APJs No. of horses No. of APJs (No. of horses)
Grade Maximum grade
0 1 2 3 0 1 2 3
NIF
 Group 1 168 20 4 0 8 4 4 0 24 (8)
 Group 2 224 20 19 13 6 3 7 7 52 (17)
 Group 3§ 300 22 53 21 1 1 16 15 96 (32)
 Group 4§ 126 17 14 11 3 1 1 9 42 (11)
Total 818 79 90 45 18 9 28 31 214 (68)
Degenerative changes
 Group 1 163 29 0 0 7 9 0 0 29 (9)
 Group 2 221 38 14 3 8 7 5 3 55 (15)
 Group 3 319 54 17 6 19 8 2 4 77 (14)
 Group 4 139 21 8 0 3 8 3 0 29 (11)
Total 842 l 42 39 9 37 32 10 7 190 (49)
Periarticular osteolysis
 Group 1 186 5 1 0 12 3 1 0 6 (4)
 Group 2 259 10 5 2 11 5 5 2 17 (12)
 Group 3§ 365 18 4 9 17 6 4 6 31 (16)
 Group 4§ 152 7 7 2 5 2 5 2 16 (9)
Total 962 40 17 13 45 16 15 10 70 (41)
Cyst-like lesions
 Group 1 189 2 1 0 14 1 1 0 3 (2)
 Group 2 257 4 12 3 15 2 3 3 19 (8)
 Group 3 384 3 7 2 24 2 5 2 12 (9)
 Group 4 159 6 2 1 8 4 1 1 9 (6)
Total 989 15 22 6 61 9 10 6 43 (25)
Fragments
 Group 1 191 0 1 0 15 0 1 0 1 (1)
 Group 2§ 258 4 9 5 13 2 5 3 18 (10)
 Group 3 384 6 3 3 27 2 2 2 12 (6)
 Group 4 162 2 3 1 10 2 1 1 6 (4)
Total 995 12 16 9 65 6 9 6 37 (21)

Indicates mean grade for the group is significantly (P < 0.05) higher, compared with group 1.

Indicates maximum grade for the group is significantly (P < 0.05) higher, compared with group 1.

See Tables 1 and 2 for remainder of key.

Size and shape of the APs—

For the horses in group 1, mean ± SD APBR was 1.0 ± 0.1 (range, 0.8 to 1.5). In the transverse images (perpendicular to the spinal cord) of these horses, the shape of the cross-sectional area of the AP was triangular for C3 through T1 and rounded for C2 through C3. For the horses in groups 2, 3, and 4, mean ± SD APBR was 1.1 ± 0.1 (0.8 to 2.4), 1.2 ± 0.1 (0.7 to 1.7), and 1.2 ± 0.1 (0.8 to 2.5), respectively.

For the case horses, mean ± SD APBR was 1.1 (0.7 to 2.5). Sixty-one APs had an APBR > 1.5, and 93.4% (57/61) APs were between C5 and T1. From C3 through T1, AP with an APBR > 1.5 had an oval to rounded cross-sectional area (Figure 2). An extra-articular dorsal bony protuberance of the caudal AP associated with the APJ was visible in 13 APJs in 8 (11.4%) case horses. This protuberance was only visible in an AP with an APBR > 1.5; C6 through C7 was affected in 11 horses and C7 through T1 in 2 horses.

Figure 2
Figure 2

Transverse CT images (in bone window) of the APJs of the cervical spine that had narrowing of the intervertebral foramen (NIF) for 3 warmblood horses. Left is to the right in the images. A—Moderate NIF caused by focal ventral bone formation of the left cranial AP of C5 (arrowhead) of the APJ of C5 through C6 for a horse that had forelimb lameness that failed to resolve following nonaxial diagnostic analgesia as its predominant clinical sign (group 3 horse). B—Moderate NIF on the left side (short line) and mild NIF on the right side (long line) caused by bilateral enlargement of the APs of the APJ of C6 through C7 for a horse that had ataxia as its predominant clinical sign (group 2 horse). Note the rounded cross-sectional area of the APs in this image, compared with the shape of the APs in panel A. A dorsal protuberance (arrowheads) is evident with each enlarged AP. Degenerative changes are not seen. C—Severe NIF on the right side caused by severe enlargement and abnormal shape of the right AP of the APJ of C6 through C7 for an ataxic horse with signs of cervical pain or stiffness as its predominant clinical sign (group 4 horse). Note the bone-to-bone contact between the AP and the endplate with adjacent sclerosis and lysis (arrowheads) and the extra-articular cyst-like lesions (arrows).

Citation: Journal of the American Veterinary Medical Association 259, 10; 10.2460/javma.20.03.0105

Assessment for NIF—

To assess NIF, the minimal distance between the APs and the adjacent vertebral body was measured, and the presence or absence of adjacent bony changes was noted (Table 1). In group 1, 168 of the 192 (87.5%) APs did not extend more ventrally than the dorsal margin of the adjacent vertebral body, and the distance between the AP and the adjacent vertebral body was > 10 mm. These foramina were not considered to be narrow. In group 1, NIF was identified for 24 (12.5%) foramina in 8 horses, with 20 foramina as grade 1 and 4 foramina as grade 2; no foramina were grade 3. In the case horses, NIF was identified for 190 (22.3%) foramina in 60 (85.7%) horses. Specifically, in group 2, NIF was identified for 52 (18.8%) foramina in 17 (73.9%) horses. In group 3, NIF was identified for 96 (24.2%) foramina in 32 (97.7%) horses. In group 4, NIF was identified for 42 (25.2%) foramina in 11 (78.6%) horses. Several sites of NIF were identified in 43 of these 60 (71.7%) horses. The cause of NIF was global enlargement of the AP for 172 of these 190 (90.5%) foramina and extra-articular focal ventral bone formation for 18 (9.5%) foramina (Figure 2). For 150 of these 190 (78.9%) foramina, NIF was bilateral.

Degenerative changes of the APJs—

In group 1, the subchondral bone plate was mildly thickened toward the medial aspect of the APJ, and the articular surfaces of the cranial and caudal AP could not be distinguished. Degenerative changes were identified in 29 (15.1%) APJs in 9 horses (Tables 2 and 3). These 9 horses had grade 1 degenerative changes and several affected APJs. No horse had grade 2 or grade 3 degenerative changes.

In the case horses, degenerative changes were identified in 161 (19.2%) APJs in 40 (57.1%) horses (Figure 3). Specifically, in group 2, degenerative changes were identified in 55 (20%) APJs in 15 (65.2%) horses. In group 3, degenerative changes were identified in 77 (19.4%) APJs in 14 (42.4%) horses. In group 4, degenerative changes were identified in 29 (17.3%) APJs in 11 (78.6%) horses.

Figure 3
Figure 3

Computed tomographic images (in bone window) of the APJs of the cervical spine that have suspected degenerative changes for 4 warmblood horses. Left is to the right in the images. A—Transverse image of the APJ of C4 through C5 for a group 4 horse. Note the osteophyte of the right caudal AP of C4 (arrow) and the dorsal protuberance associated with each AP (arrowheads). B—Transverse image of the APJ of C5 through C6 for a group 3 horse. Note the osteophyte of the left caudal AP of C5 (arrow) and subchondral bone sclerosis (arrowheads). C—Reconstructed CT image of the APJ of C3 through C4 in a dorsal plane for a group 3 horse. Cranial is to the top of the image. Note the osteophytes at the lateral aspect of the caudal APs of C3 (arrowheads). D—Transverse image of the APJ of C5 through C6 for a group 4 horse. Note the severe degenerative changes: decrease in the size of the joint space, periarticular gas attenuation (arrowheads), and severe sclerosis (black arrows) and lysis (white arrows) of the left cranial AP of C6.

Citation: Journal of the American Veterinary Medical Association 259, 10; 10.2460/javma.20.03.0105

Periarticular osteolysis—

To assess periarticular osteolysis, the number and depth of the bony defects were determined (Table 1). In group 1, periarticular osteolysis was detected in 6 (3.8%) APJs in 4 horses. Five APJs had grade 1 periarticular osteolysis, and 1 APJ had grade 2; no horse had grade 3. In the case horses, periarticular osteolysis was detected in 64 (7.6%) APJs in 37 (52.9%) horses. Specifically, periarticular osteolysis was identified in 17 (6.2%) APJs in 12 (52.2%) group 2 horses, in 31 (7.8%) APJs in 16 (48.5%) group 3 horses, and in 16 (9.5%) APJs in 9 (64.3%) group 4 horses. The APJ of C6 through C7 was affected in 48 of these 64 (75%) horses. Osteolysis was always identified in the pedicle or body of the cranial vertebra of the APJ or in the dorsal lamina of the caudal vertebra of the APJ (Figure 4). The adjacent spinous processes were also involved in 4 horses. In all horses, an illdefined area of reduced attenuation in the soft tissue was visible adjacent to the sites of osteolysis. Five APJs with grade 3 periarticular osteolysis had multifocal mineral attenuation in this area of soft tissue attenuation.

Figure 4
Figure 4

Computed tomographic images (in bone [A through C] or soft tissue [D] window) of the APJs of the cervical spine that have periarticular osteolysis for 4 warm-blood horses. Left is to the right in the transverse images (A, C, and D), and cranial is to the left in the sagittal image (B). A—Transverse image of the APJ of C6 through C7 for a group 3 horse. Note osteolysis cranioventral to the right APs (black arrowheads) and the absence of the ventral lamina of C6 on the right (arrow) because of transposition of the C6 ventral lamina to C7. B—Reconstructed image of C5 through T1 in a sagittal plane of another group 3 horse. Note NIF at the cranial aspects of C6 and C7 (arrows) and the small fragment at the dorsal aspect of the intervertebral symphysis of C7 through T1 (white arrowhead). C—Transverse image of the APJ of C6 through C7 for a group 4 horse. Note the severe osteolysis and accompanying sclerosis (arrowheads) caudal to the left AP. D— Transverse image of C6 for a group 3 horse. Note osteolysis of the left pedicle of C6 and decreased attenuation (attenuation value, 43 HU) of the adjacent soft tissues (arrow), compared with the rest of the soft tissue, including adjacent to the right side of C6 (attenuation value, 92 HU), and mineral attenuation in the soft tissue ventral to the area of soft tissue with decreased attenuation (arrowheads).

Citation: Journal of the American Veterinary Medical Association 259, 10; 10.2460/javma.20.03.0105

Cyst-like lesions of the APs—

To assess the cyst-like lesions of the AP, their number and size were noted (Table 1). In group 1, cyst-like lesions were identified in 3 (1.6%) APJs in 2 horses. Two APJs had a grade 1 cyst-like lesion, and 1 APJ had grade 2; no APJ had grade 3. In the case horses, cyst-like lesions were identified in 40 (4.8%) APJs in 23 (27.3%) horses (Figure 5). Specifically, cyst-like lesions were identified in 19 (6.9%) APJs in 8 (34.8%) group 2 horses, in 12 (3%) APJs in 9 (27.3%) group 3 horses, and in 9 (5.4%) APJs in 6 (42.9%) group 4 horses. The caudal region of the cervical spine and specifically C6 through C7 were involved in 32 (80%) and 16 (40%) of these 40 APJs, respectively. Only 1 APJ was affected in 14 of these 23 (60.9%) horses, whereas the remaining 9 horses had ≥ 2 APJs that were affected. Identified types of cyst-like lesions in the 40 APJs were as follows: circumscribed lesion without evidence of communication with the joint (n = 6), lesion with an extra-articular opening (7), lesion with an articular opening (15), and lesions that were a combination of the aforementioned types (12).

Figure 5
Figure 5

Computed tomographic images (in bone window) of the APJs of the cervical spine that have cyst-like lesions or fragments of the APs for 4 warmblood horses. Left is to the right (A, B, and D) and cranial is to the top (C) in the images. A—Trans-verse image of the APJ of C2 through C3 for a group 3 horse. Note the small intra-articular fragment and adjacent subchondral bone defect (arrowhead). B—Transverse image of the APJ of C3 through C4 for a group 4 horse. Note a large cyst-like lesion (arrowheads) that interrupts the subchondral bone plate with the joint space. C—Reconstructed CT image of C5 and C6 in a dorsal plane for another group 3 horse. At C5 through C6, note the rounded fragment with a hypoattenuating core (arrowhead). Also note the periarticular osteolysis just cranial to the left AP of C6 through C7 (arrow). D— Transverse image of the APJ of C5 through C6 for a group 4 horse. Note the cyst-like lesions and severe fragmentation of the left AP and severe enlargement of both APs.

Citation: Journal of the American Veterinary Medical Association 259, 10; 10.2460/javma.20.03.0105

Fragmentation of the APs—

The number and size of the fragments were determined (Table 1). In group 1, a grade 2 fragment was identified in 1 (0.5%) APJ in 1 (6.3%) horse; no horse had a grade 1 or 3 fragment. In the case horses, fragments were detected in 36 (4.3%) APJs in 20 (28.6%) horses (Figure 5). Specifically, fragments were identified in 18 (6.5%) APJs in 10 (43.5%) group 2 horses, in 12 (3%) APJs in 6 (18.2%) group 3 horses, and in 6 (3.6%) APJs in 4 (28.6%) group 4 horses. The caudal region of the cervical spine and specifically C7 through T1 were involved in 29 (80.6%) and 18 (50%) of these 36 APJs, respectively. Only 1 APJ was affected in 11 of these 20 horses, whereas the remaining 9 horses had ≥ 2 affected APJs. Identified types of fragments in the 36 APJs were as follows: intra-articular fragment without or with a minimal defect of the subchondral bone (n = 6), fragment without involvement of the subchondral bone (11), fragment with involvement of the subchondral bone (7), and fragment that was a combination of the aforementioned types (12). One fragment was removed arthroscopically and had macroscopic characteristics of a fragment.

Association between CT findings and clinical signs—

Horses were more likely to belong to group 2 rather than to group 1 with increasing maximum (P = 0.047) and mean (P = 0.03) grade of fragmentation. Horses were more likely to belong to group 3 rather than to group 1 with increasing maximum and mean APBR (P < 0.001), increasing maximum and mean grade of NIF (P < 0.001), and increasing mean grade of periarticular osteolysis (P = 0.007). Horses were more likely to belong to group 4 rather than to group 1 with increasing maximum (P < 0.001) and mean (P = 0.016) APBR, increasing maximum (P = 0.004) and mean (P = 0.004) grade of NIF, and increasing maximum (P = 0.012) and mean (P = 0.011) grade of periarticular osteolysis. For group 3, maximum (70.1%) and mean (70.8%) grades of NIF were significantly (P = 0.037 and P = 0.021, respectively) higher ipsilateral to the affected (lame) limb.

Factors influencing the APBR—

Significant positive correlations were noted between APBR and grade of NIF (P < 0.001), grade of degenerative changes (P = 0.003), or presence of focal ventral bone formation (P < 0.001). Mean ± SD APBR of C6 through C7 (1.3 ± 0.019) was significantly (P < 0.001 for all pairwise comparisons) higher than all other APJs (C2 through C3, 1.0 ± 0.024; C3 through C4, 0.9 ± 0.241; C4 through C5, 1.1 ± 0.024; C5 through C6, 1.13 ± 0.019; and C7 through T1, 1.1 ± 0.019). With exclusion of C6 through C7, APBR of C5 through C6 was also significantly (P ≤ 0.039 for all pairwise comparisons) higher than all other APJs. The APBRs between C2 and C3, C3 and C4, C4 and C5, and C7 and T1 were not significantly (P ≥ 0.344 for all pairwise comparisons) different.

Age (P = 0.223), sex (male, 1.1 ± 0.016; female, 1.1 ± 0.024; P = 0.084), and the side of the affected APJ (left, 1.1 ± 0.016; right, 1.1 ± 0.016; P = 0.123) did not have a significant effect on APBR. The percentages of APJs with APBRs > 1.5 that did not have any degenerative changes, periarticular osteolysis, or both were 61.5%, 46.2%, and 32.3%, respectively.

Discussion

The objectives of the retrospective study reported here were to describe antemortem CT findings of diseased APJs of the cervical spine in a large group of horses and to investigate whether CT findings were associated with specific clinical signs. Computed tomography was confirmed, as expected, to be a useful modality to identify lesions of the APJs of the cervical spine, and an association was confirmed, as expected, between CT findings and clinical signs. Acquisition of CT images of the cervical spine was successful for all horses with the CT machine used in this study. It had a standard aperture diameter of 72 cm and had a limited amount of hardware between the horse's shoulders and the bore of the device.

Horses that had high APBR and grades of periarticular osteolysis and NIF were significantly more likely to belong to groups 3 (forelimb lameness) or 4 (signs of cervical pain or stiffness). Horses with a high grade of AP fragmentation were significantly more likely to belong to group 2 (ataxia). The reason that fragmentation of an AP primarily caused ataxia without any other significant differences in the APs (eg, differences in APBRs or grade of periarticular osteolysis) between groups 1 and 2 is unclear. However, no significant differences were identified in the grade of AP fragmentation between group 1 and groups 3 or 4 and in the grade of cyst-like lesions between control and case groups (combined group 2, 3, and 4 horses).

The present study did not reveal any association between age, sex, and APBR. The APBRs for C5 through C6 and C6 through C7 were significantly higher, compared with the APBRs for other vertebrae. These results agreed with the results of a radiographic study19 with the exception of finding a positive correlation between the age of a horse and the size of the C5-C6 APJ (ie, as a horse ages, the APJ increases in size) in that study. This discrepancy between studies is likely because of the difference in imaging modalities (CT vs radiography). Computed tomography is believed to be more accurate than radiography to assess AP size owing to its higher contrast resolution and ability to evaluate the cervical spine in multiple planes. Focal ventral extra-articular bone formation or the presence of a dorsal protuberance was identified in case horses, and the presence of these features may lead to an overestimation of the size of an AP as determined radiographically. Moreover, differentiating an enlarged APJ with NIF from one without NIF radiographically is impossible when the ventral portion of an AP is superimposed on a foramen.

With the exception of the degenerative changes, all the abnormalities of the APJs were more frequently identified in the caudal portion of the cervical spine. The increased range of motion and mechanical load imposed on the caudal portion were the most likely explanations for this finding.17

Periarticular osteolysis of the APJ was detected in 52.9% of the case horses, and C6 through C7 was more frequently affected than any other APJ. Osteolysis was always in the pedicle of the cranial vertebra or the dorsal lamina of the caudal vertebra of the APJ. A literature search did not reveal any previous reports of periarticular osteolysis of the APJs of the cervical spine of horses. Periarticular osteolysis may have developed secondary to pressure from chronic distention of the APJ with synovial fluid because the sites of osteolysis were adjacent to areas of decreased soft tissue attenuation, consistent with the location of artificially distended APJ pouches in a study13 of cadaveric horses. Five horses with grade 3 osteolysis had multifocal mineral attenuation in the soft tissue adjacent to the lytic site. This was consistent with dystrophic mineralization of the APJ capsule or mineralization following corticosteroid injection in the APJ. However, whether these horses received an intra-articular injection of corticosteroid was unknown.

For the case horses, an association was not evident between age and size of the APJ, and 32.3% of the APs with APBRs > 1.5 did not have any degenerative changes or periarticular osteolysis. Enlarged and remodeled APJs have been linked to several pathologic processes including vertebral malformations3,7,20 and osteoarthrosis.2,19 For the case horses of the present study, a developmental or congenital origin, such as dysplasia or osteochondrosis, was suspected as the cause of enlarged and misshaped APs without concurrent degenerative changes of the corresponding APJs. The presence of osteochondrosis would be consistent with a report20 of Thoroughbred horses in which all superficial lesions that involved the APs had histologic features of osteochondrosis. However, a strong correlation was identified between size of the APJ and grade of degenerative changes for the case horses in the present study. Enlarged APJs were speculated to be more prone to undergo degeneration because of an alteration of their biomechanics.

Osseous cyst-like lesions and fragmentation of the AP were detected in 32.9% and 28.6% of cases, respectively. The most common location for a cyst-like lesion was C6 through C7 and for fragmentation was C7 through T1. On the basis of the CT findings in the present study and in previous reports,16,20,21 most cyst-like lesions and fragments in the cases were likely a manifestation of osteochondrosis. However, histologic evaluation is needed to confirm that cyst-like lesions are a manifestation of osteochondrosis. Other suspected causes included trauma, degeneration, vascular malformations, hemorrhage, ischemic necrosis, occlusion of venous drainage, or other developmental abnormalities.20,21

Narrowing of the intervertebral foramen was detected in 85.7% of cases. The most common cause was global enlargement of the APJ (90.5%), followed by focal ventral bone formation. Horses with forelimb lameness or cervical pain or stiffness were more likely to have NIF and were suspected to have a radiculopathy secondary to impingement of the spinal nerves. However, the presence of radiculopathy was only suspected, not confirmed, because the cervical spinal nerves could not be clearly seen in the CT images despite the use of a soft tissue reconstruction filter, windowing, and leveling. Moreover, NIF was evaluated by measuring the minimum distance between an AP and its adjacent vertebrae; however, the cervical spinal nerves have a caudolateral direction and the nerves exit the intervertebral foramina caudally.17,18 Therefore, NIF in the cranial direction may not cause impingement of the spinal nerves. As mentioned for assessment of the cervical spinal nerves, assessment of spinal cord compression was not possible because of a lack of soft tissue contrast, despite use of the soft tissue reconstruction filter, windowing, and leveling.

A critical limitation of the present study was that no functional diagnostic technique was included to objectively support the clinical relevance of the CT findings. Diagnostic analgesia of the APJ, magnetic evoked potentials, transcranial electrical stimulation, electromyography, scintigraphy, and ultrasound examination could have been performed to further rule out other pathologic changes, confirm the diagnosis, and evaluate functional integrity of the spinal cord.2,9,22,23 However, these techniques (ultrasonography or scintigraphy) were used inconsistently in our cases. This limitation was because this study was retrospective. Another limitation was the lack of a postmortem examination. Postmortem data were usually difficult to obtain from client-owned horses, and further studies correlating the CT findings with postmortem data are warranted.

In conclusion, CT of the entire cervical spine was feasible for the warmblood horses of the present study, and acquired images were useful for evaluating the APJs of the cervical spine. The main identified abnormalities were NIF, degenerative changes, periarticular osteolysis, osseous cyst-like lesions, and fragmentation of the APJ, and the APs were of various sizes and shapes. An association was found between the CT findings and clinical signs. Further studies are required to evaluate the usefulness of contrast-enhanced diagnostic imaging techniques, correlate CT and histologic findings, and further evaluate the clinical relevance of pathologic changes of the APJs of the cervical spine.

Acknowledgments

No external funding was used in this study. The authors declare that there were no conflicts of interest.

The authors thank Drs. Taylor and Houdellier for their contributions to this study.

References

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Contributor Notes

Address correspondence to Dr. Rovel (rovel.tibor@gmail.com).
  • Figure 1

    Representative CT images (in bone window), with orientation of the images controlled by use of multiplanar reconstruction, of the C4-C5 articular process joint (APJ; A and B) and C6 vertebra (C) of a warmblood horse of the control group that illustrate the landmarks used to calculate the AP-to-vertebral body ratio. A—Transverse image at the level of the midcraniocaudal aspect of the C4-C5 APJ. Right is at the left of the image. The midcraniocaudal aspect of C4 through C5 was identified by scrolling through the images in a craniocaudal direction. After the image was selected, the closed polygon function of the DICOM viewer (Osirix; Pixmeo SARL) was used to measure the cross-sectional area of the left and right APs. On both sides, the cranial and caudal APs were measured together. B—Transverse image at the level of the maximum cross-sectional area of the cranial aspect of the body of C6. Right is at the left of the image. The maximum cross-sectional area was determined by scrolling through the images in a craniocaudal direction in the area of the body cranial to the origin of the vertebral pedicles to visualize the maximum area. After the image was selected, the closed polygon function of the DICOM viewer was used to measure the cross-sectional area. C—Sagittal image with a purple line that indicates the level of C6 in panel B. The blue line demarcates the dorsal surface of the body of C6, and the purple line is perpendicular to the blue line.

  • Figure 2

    Transverse CT images (in bone window) of the APJs of the cervical spine that had narrowing of the intervertebral foramen (NIF) for 3 warmblood horses. Left is to the right in the images. A—Moderate NIF caused by focal ventral bone formation of the left cranial AP of C5 (arrowhead) of the APJ of C5 through C6 for a horse that had forelimb lameness that failed to resolve following nonaxial diagnostic analgesia as its predominant clinical sign (group 3 horse). B—Moderate NIF on the left side (short line) and mild NIF on the right side (long line) caused by bilateral enlargement of the APs of the APJ of C6 through C7 for a horse that had ataxia as its predominant clinical sign (group 2 horse). Note the rounded cross-sectional area of the APs in this image, compared with the shape of the APs in panel A. A dorsal protuberance (arrowheads) is evident with each enlarged AP. Degenerative changes are not seen. C—Severe NIF on the right side caused by severe enlargement and abnormal shape of the right AP of the APJ of C6 through C7 for an ataxic horse with signs of cervical pain or stiffness as its predominant clinical sign (group 4 horse). Note the bone-to-bone contact between the AP and the endplate with adjacent sclerosis and lysis (arrowheads) and the extra-articular cyst-like lesions (arrows).

  • Figure 3

    Computed tomographic images (in bone window) of the APJs of the cervical spine that have suspected degenerative changes for 4 warmblood horses. Left is to the right in the images. A—Transverse image of the APJ of C4 through C5 for a group 4 horse. Note the osteophyte of the right caudal AP of C4 (arrow) and the dorsal protuberance associated with each AP (arrowheads). B—Transverse image of the APJ of C5 through C6 for a group 3 horse. Note the osteophyte of the left caudal AP of C5 (arrow) and subchondral bone sclerosis (arrowheads). C—Reconstructed CT image of the APJ of C3 through C4 in a dorsal plane for a group 3 horse. Cranial is to the top of the image. Note the osteophytes at the lateral aspect of the caudal APs of C3 (arrowheads). D—Transverse image of the APJ of C5 through C6 for a group 4 horse. Note the severe degenerative changes: decrease in the size of the joint space, periarticular gas attenuation (arrowheads), and severe sclerosis (black arrows) and lysis (white arrows) of the left cranial AP of C6.

  • Figure 4

    Computed tomographic images (in bone [A through C] or soft tissue [D] window) of the APJs of the cervical spine that have periarticular osteolysis for 4 warm-blood horses. Left is to the right in the transverse images (A, C, and D), and cranial is to the left in the sagittal image (B). A—Transverse image of the APJ of C6 through C7 for a group 3 horse. Note osteolysis cranioventral to the right APs (black arrowheads) and the absence of the ventral lamina of C6 on the right (arrow) because of transposition of the C6 ventral lamina to C7. B—Reconstructed image of C5 through T1 in a sagittal plane of another group 3 horse. Note NIF at the cranial aspects of C6 and C7 (arrows) and the small fragment at the dorsal aspect of the intervertebral symphysis of C7 through T1 (white arrowhead). C—Transverse image of the APJ of C6 through C7 for a group 4 horse. Note the severe osteolysis and accompanying sclerosis (arrowheads) caudal to the left AP. D— Transverse image of C6 for a group 3 horse. Note osteolysis of the left pedicle of C6 and decreased attenuation (attenuation value, 43 HU) of the adjacent soft tissues (arrow), compared with the rest of the soft tissue, including adjacent to the right side of C6 (attenuation value, 92 HU), and mineral attenuation in the soft tissue ventral to the area of soft tissue with decreased attenuation (arrowheads).

  • Figure 5

    Computed tomographic images (in bone window) of the APJs of the cervical spine that have cyst-like lesions or fragments of the APs for 4 warmblood horses. Left is to the right (A, B, and D) and cranial is to the top (C) in the images. A—Trans-verse image of the APJ of C2 through C3 for a group 3 horse. Note the small intra-articular fragment and adjacent subchondral bone defect (arrowhead). B—Transverse image of the APJ of C3 through C4 for a group 4 horse. Note a large cyst-like lesion (arrowheads) that interrupts the subchondral bone plate with the joint space. C—Reconstructed CT image of C5 and C6 in a dorsal plane for another group 3 horse. At C5 through C6, note the rounded fragment with a hypoattenuating core (arrowhead). Also note the periarticular osteolysis just cranial to the left AP of C6 through C7 (arrow). D— Transverse image of the APJ of C5 through C6 for a group 4 horse. Note the cyst-like lesions and severe fragmentation of the left AP and severe enlargement of both APs.

  • 1.

    Hahn CN, Handel I, Green SL, Bronsvoort MB, Mayhew IG. Assessment of the utility of using intra- and intervertebral minimum sagittal diameter ratios in the diagnosis of cervical vertebral malformation in horses. Vet Radiol Ultrasound. 2008;49(1):16. doi:10.1111/j.1740-8261.2007.00308.x

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2.

    Dyson SJ. Lesions of the equine neck resulting in lameness or poor performance. Vet Clin North Am Equine Pract. 2011;27(3):417437. doi:10.1016/j.cveq.2011.08.005

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3.

    Hoffman CJ, Clark CK. Prognosis for racing with conservative management of cervical vertebral malformation in Thoroughbreds: 103 cases (2002–2010). J Vet Intern Med. 2013;27(2):317323. doi:10.1111/jvim.12053

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4.

    Didierlaurent D, Contremoulins V, Denoix JM, Audigié F. Scintigraphic pattern of uptake of 99mTechnetium by the cervical vertebrae of sound horses. Vet Rec. 2009;164(26):809813. doi:10.1136/vr.164.26.809

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5. Butler JA, Colles CM, Dyson SJ, et al. Clinical radiology of the horse. In: Butler JA, Colles CM, Dyson SJ, et al., eds. Clinical Radiology of the Horse. 4th ed. Wiley-Blackwell; 2017:531607.

    • Search Google Scholar
    • Export Citation
  • 6.

    Moore BR, Reed SM, Robertson JT. Surgical treatment of cervical stenotic myelopathy in horses: 73 cases (1983–1992). J Am Vet Med Assoc. 1993;203(1):108112.

    • Search Google Scholar
    • Export Citation
  • 7.

    Moore BR, Holbrook TC, Stefanacci JD, Reed SM, Tate LP, Menard MC. Contrast-enhanced computed tomography and myelography in six horses with cervical stenotic myelopathy. Equine Vet J. 1992;24(3):197202. doi:10.1111/j.2042-3306.1992.tb02814.x

    • Crossref
    • Search Google Scholar
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  • 8.

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