Introduction
The lumbosacral (LS) and sacroiliac regions in horses are of interest in fields of biomechanics and locomotor pathology, and pain associated with the lumbar and LS regions of the vertebral column is a common cause of poor performance and lack of power in the hind limbs of horses.1,2,3,4,5,6 The LS articulation7 comprises the LS intervertebral symphysis (which includes the L5-S1 or L6-S1 intervertebral disc [IVD]), bilateral intertransverse and articular processes joints, and syndesmoses.8,9,10 Anatomic variations of the LS articulation have been described in horses in postmortem studies11,12 and with the use of in vivo transrectal ultrasonography.6,13,14,15,16 These anatomic variations may affect mobility, function, performance, and pathological processes in horses.12
Diagnostic imaging modalities useful to assess the LS articulation in horses are limited. For instance, although lateral radiographic images of the LS region in a standing horse can be acquired with a powerful radiographic machine, the superimposition of the tubera coxae severely diminishes the diagnostic value of this radiographic projection, and informative radiographic examination of the LS region requires a ventrodorsal projection, with the horse anesthetized and positioned in dorsal recumbency.16,17,18 Additionally, this ventrodorsal view has limited clinical usefulness in evaluating structures of interest because of superimposition of abdominal viscera; thus, radiography is not routinely used.18 Radiation capture in nuclear scintigraphy is limited for the LS intervertebral symphysis because of its deep position at the ventral aspect of the vertebral column but is easy for the dorsal aspects, such as the lumbar and sacral vertebral spinous processes. With the use of transrectal ultrasonography, historically, we had identified many horses with LS synostosis (fusion of vertebral bodies of the caudalmost lumbar vertebra and S1) of various degrees, from mild partial dorsal synostosis to complete synostosis, and we noticed that the extent of synostosis often corresponded with the caudal angulation of the caudalmost lumbar spinous process, as seen on scintigraphic images. Variations in the orientation of the vertebral spinous processes at the LS articulation have been reported.11,12 One study12 shows that variations of the LS intervertebral symphysis depend on the presence or absence of an LS IVD. In vivo studies6,19,20 of transrectal ultrasonographic assessment of the LS intervertebral symphysis in horses show differences in frequency of occurrence of LS anatomic variations among breeds. Additionally, Tallaj et al21 reported that the shape of the sacroiliac joints differed for horses grouped on the basis of sex; however, sex predisposition for LS anatomic variations was not specifically investigated.
The general objectives of the retrospective study reported here were to evaluate whether the angulation of the caudalmost lumbar spinous process evident on nuclear scintigraphy (scintigraphic type [1a, 1b, 2, or 3]) would correlate with the grade of anatomic variant of the LS intervertebral symphysis evident on transrectal ultrasonography (ultrasonographic grade [1, 2, or 3]) and to describe the occurrence of these variants among horses grouped on the basis of sex or breed for 3 breeds that predominate in France in sport and racing disciplines: the Selle Français Warmblood (SF), French Standardbred Trotter (FT), and Thoroughbred (TB). Therefore, our 3 main objectives were to create a classification system to evaluate LS anatomic variants with nuclear scintigraphy, describe anatomic variants of the LS articulation evident with nuclear scintigraphy and transrectal ultrasonography for horses grouped on the basis of sex and breed, and evaluate the agreement between findings from nuclear scintigraphy and those from transrectal ultrasonography to describe these anatomic variations. We hypothesized that the angulation of the spinous process of the caudalmost lumbar vertebra identified on nuclear scintigraphy would correspond with the LS symphysis anatomic variant identified on transrectal ultrasonography such that the scintigraphic type 1 would be associated with the ultrasonographic grade 1 and, similarly, type 2 with grade 2 and type 3 with grade 3. Such data could help to discriminate anatomic variants from clinically important pathological findings.
Materials and Methods
Sample population and inclusion criteria
The clinical records database of the Centre de Recherche et d’Imagerie des Affections Locomotrices Equines was searched for records of FTs, SFs, and TBs that had undergone nuclear scintigraphy and transrectal ultrasonography of the lumbar and LS regions of the vertebral column between January 2016 and December 2019. These 3 breeds were selected because they predominate in France and are used in various sports (SFs) and racing (FTs and TBs). Horses were excluded if they had an incomplete clinical record (eg, if ultrasonographic images were missing) or if images were of poor quality (eg, blurry ultrasonographic images or scintigraphic images with a poor signal-to-noise ratio or interference associated with an excessive volume of urine in the bladder).
On the basis of results from a preliminary study performed on 100 horses (34 SFs, 33 FTs, and 33 TBs) to determine expected prevalences of LS anatomic variants identified on nuclear scintigraphy, power analysis indicated that inclusion of a minimum of 239 horses was necessary to reach 80% power for statistical agreement tests.22 Because sex was previously reported to influence the shape of sacroiliac joints,21 we randomly selected 27 sexually intact females, 27 sexually intact males, and 27 geldings (a total of 81 horses) for each of the 3 breeds for uniformity across groups.
Nuclear scintigraphy
Acquisition and motion correction
For skeletal scintigraphic examination of the vertebral column and pelvis, each horse first had been lunged for 15 minutes immediately before technetium Tc 99m dicarboxypropane diphosphonate (Curium Pharma; 1 GBq/100 kg, IV) was administered; bone-phase nuclear scintigraphy was conducted 3 hours later. Depending on the horse’s behavior, sedation with detomidine hydrochloride (10 to 15 μg/kg, IV) and morphine hydrochloride (20 or 40 mg, IV) was administered. Scintigraphic images were obtained with a γ camera (Millenium MPR; GE Healthcare) equipped with a low-energy, high-resolution collimator. The rectangular field of view was 520 × 370 mm. Each dynamic acquisition image was obtained with 30 frames, each of 2 seconds’ duration and 128 × 128 matrix size. Each dynamic acquisition underwent motion correction, as previously described,23 to yield a static image. For each horse, 6 static images were evaluated: 1 each of standing dorsal, left dorso-45°-lateral oblique, and right dorso-45°-lateral oblique that spanned from the thoracolumbar vertebral articulation to the level of the cranial margin of the tubera sacrale and 1 each of standing dorso-20°-caudal oblique, left dorso-45°-lateral oblique, and right dorso-45°-lateral oblique of the pelvis from the cranial aspects of the tubera coxae to the caudal aspects of the tubera ischiadica (Figure 1), as previously described.24
Representative clinical photographs of γ-camera positioning (A through D) for the corresponding nuclear scintigraphic images acquired (E through H) 3 hours after administration of technetium Tc 99m dicarboxypropane diphosphonate to 1 of 243 horses (81 Selle Français Warmbloods, 81 French Standardbred Trotters, and 81 Thoroughbreds) between January 2016 and December 2019 for examination of the lumbar and sacral vertebrae and pelvis, showing the dorsal (A and E) and left dorso-45°-lateral oblique (B and F) plane images of the vertebral column from the thoracolumbar articulation to the cranial margin of the tubera sacrale and the dorso-20°-caudal oblique (C and G) and left dorso-45°-lateral oblique (D and H) plane images of the vertebral column from the level of the cranial aspect of both tubera coxae to the caudal aspect of both tubera ischiadica. The color scale on the right of panel E represents radiopharmaceutical uptake (photon count range, 0 [black] to maximum count [145; white]) evident on each of the scintigraphic images.
Citation: Journal of the American Veterinary Medical Association 260, 1; 10.2460/javma.20.08.0428
Representative clinical photographs of γ-camera positioning (A through D) for the corresponding nuclear scintigraphic images acquired (E through H) 3 hours after administration of technetium Tc 99m dicarboxypropane diphosphonate to 1 of 243 horses (81 Selle Français Warmbloods, 81 French Standardbred Trotters, and 81 Thoroughbreds) between January 2016 and December 2019 for examination of the lumbar and sacral vertebrae and pelvis, showing the dorsal (A and E) and left dorso-45°-lateral oblique (B and F) plane images of the vertebral column from the thoracolumbar articulation to the cranial margin of the tubera sacrale and the dorso-20°-caudal oblique (C and G) and left dorso-45°-lateral oblique (D and H) plane images of the vertebral column from the level of the cranial aspect of both tubera coxae to the caudal aspect of both tubera ischiadica. The color scale on the right of panel E represents radiopharmaceutical uptake (photon count range, 0 [black] to maximum count [145; white]) evident on each of the scintigraphic images.
Citation: Journal of the American Veterinary Medical Association 260, 1; 10.2460/javma.20.08.0428
Representative clinical photographs of γ-camera positioning (A through D) for the corresponding nuclear scintigraphic images acquired (E through H) 3 hours after administration of technetium Tc 99m dicarboxypropane diphosphonate to 1 of 243 horses (81 Selle Français Warmbloods, 81 French Standardbred Trotters, and 81 Thoroughbreds) between January 2016 and December 2019 for examination of the lumbar and sacral vertebrae and pelvis, showing the dorsal (A and E) and left dorso-45°-lateral oblique (B and F) plane images of the vertebral column from the thoracolumbar articulation to the cranial margin of the tubera sacrale and the dorso-20°-caudal oblique (C and G) and left dorso-45°-lateral oblique (D and H) plane images of the vertebral column from the level of the cranial aspect of both tubera coxae to the caudal aspect of both tubera ischiadica. The color scale on the right of panel E represents radiopharmaceutical uptake (photon count range, 0 [black] to maximum count [145; white]) evident on each of the scintigraphic images.
Citation: Journal of the American Veterinary Medical Association 260, 1; 10.2460/javma.20.08.0428
Image interpretation
Each set of static scintigraphic images was anonymized for all horses, and the order in which they were evaluated was completely randomized by means of random permutation to avoid bias during evaluations by reviewers. Images were reviewed independently by a senior veterinary radiology specialist and large animal associate member of the European College of Veterinary Diagnostic Imaging who was experienced in evaluating scintigraphic images (FA) and a veterinary specialist in locomotor pathology (GV). Both observers were blinded to the other’s results.
Each observer was asked to review the scintigraphic images for each horse and categorize horses according to a classification system we developed for our study. This classification system consisted of 4 scintigraphic types (1a, 1b, 2, or 3) assigned on the basis of anatomic variant characteristics of lumbar and LS vertebral conformation, with the number of true lumbar vertebrae present and the angulation of the spinous processes of the most caudal lumbar vertebrae and S1 (Figures 2 and 3).
Schematic image showing 4 anatomic lumbosacral (LS) variants evident on dorsal plane nuclear scintigraphic images of the LS and pelvic regions of the horses described in Figure 1, with classification of scintigraphic type (1a, 1b, 2, or 3) based on the number of true lumbar vertebrae (ie, 5 [types 1b and 3] vs 6 [types 1a and 2]), location of the dorsal aspect of the spinous process of the caudalmost lumbar vertebra (L5 [bright pink] vs L6 [blue]) relative to the tubera sacrale (gray), distance between the spinous processes of the 2 most caudal lumbar vertebrae (double arrow a), and distance between L6 and S1 (double arrow b). For each depiction, the horse’s head is toward the top and its left side is toward the left of the image. In type 1a, the dorsal aspect of the L6 spinous process is cranial to the tubera sacrale, and distance a < distance b. Type 1a is the typical anatomic conformation previously described.9,24 Type 1b has only 5 true lumbar vertebrae (ie, either no L6 or a transitional L1), the dorsal aspect of the spinous process of L5 is cranial to the tubera sacrale, and the distance between the spinous processes is shorter for the 2 most caudal lumbar vertebrae than for L5 and S1 (similar to the LS articulation in type 1a). In type 2, the dorsal aspect of the L6 spinous process is located in the cranial half of the intersacral space (diagonal lines) and a ≃ b. Type 3 has only 5 true lumbar vertebrae and LS synostosis (fusion of L6 and S1), the dorsal aspect of the L6 spinous process is in the caudal half of the intersacral space, and a > b.
Citation: Journal of the American Veterinary Medical Association 260, 1; 10.2460/javma.20.08.0428
Schematic image showing 4 anatomic lumbosacral (LS) variants evident on dorsal plane nuclear scintigraphic images of the LS and pelvic regions of the horses described in Figure 1, with classification of scintigraphic type (1a, 1b, 2, or 3) based on the number of true lumbar vertebrae (ie, 5 [types 1b and 3] vs 6 [types 1a and 2]), location of the dorsal aspect of the spinous process of the caudalmost lumbar vertebra (L5 [bright pink] vs L6 [blue]) relative to the tubera sacrale (gray), distance between the spinous processes of the 2 most caudal lumbar vertebrae (double arrow a), and distance between L6 and S1 (double arrow b). For each depiction, the horse’s head is toward the top and its left side is toward the left of the image. In type 1a, the dorsal aspect of the L6 spinous process is cranial to the tubera sacrale, and distance a < distance b. Type 1a is the typical anatomic conformation previously described.9,24 Type 1b has only 5 true lumbar vertebrae (ie, either no L6 or a transitional L1), the dorsal aspect of the spinous process of L5 is cranial to the tubera sacrale, and the distance between the spinous processes is shorter for the 2 most caudal lumbar vertebrae than for L5 and S1 (similar to the LS articulation in type 1a). In type 2, the dorsal aspect of the L6 spinous process is located in the cranial half of the intersacral space (diagonal lines) and a ≃ b. Type 3 has only 5 true lumbar vertebrae and LS synostosis (fusion of L6 and S1), the dorsal aspect of the L6 spinous process is in the caudal half of the intersacral space, and a > b.
Citation: Journal of the American Veterinary Medical Association 260, 1; 10.2460/javma.20.08.0428
Schematic image showing 4 anatomic lumbosacral (LS) variants evident on dorsal plane nuclear scintigraphic images of the LS and pelvic regions of the horses described in Figure 1, with classification of scintigraphic type (1a, 1b, 2, or 3) based on the number of true lumbar vertebrae (ie, 5 [types 1b and 3] vs 6 [types 1a and 2]), location of the dorsal aspect of the spinous process of the caudalmost lumbar vertebra (L5 [bright pink] vs L6 [blue]) relative to the tubera sacrale (gray), distance between the spinous processes of the 2 most caudal lumbar vertebrae (double arrow a), and distance between L6 and S1 (double arrow b). For each depiction, the horse’s head is toward the top and its left side is toward the left of the image. In type 1a, the dorsal aspect of the L6 spinous process is cranial to the tubera sacrale, and distance a < distance b. Type 1a is the typical anatomic conformation previously described.9,24 Type 1b has only 5 true lumbar vertebrae (ie, either no L6 or a transitional L1), the dorsal aspect of the spinous process of L5 is cranial to the tubera sacrale, and the distance between the spinous processes is shorter for the 2 most caudal lumbar vertebrae than for L5 and S1 (similar to the LS articulation in type 1a). In type 2, the dorsal aspect of the L6 spinous process is located in the cranial half of the intersacral space (diagonal lines) and a ≃ b. Type 3 has only 5 true lumbar vertebrae and LS synostosis (fusion of L6 and S1), the dorsal aspect of the L6 spinous process is in the caudal half of the intersacral space, and a > b.
Citation: Journal of the American Veterinary Medical Association 260, 1; 10.2460/javma.20.08.0428
Representative paired dorsal (top) and dorso-20°-caudal oblique (bottom) nuclear scintigraphic images of horses described in Figure 1, showing the scintigraphic types (type 1a [A], type 1b [B], type 2 [C], and type 3 [D]) described in Figure 2. In all images, the horse’s left side is toward the left and cranial is toward the top. Notice that the S1 spinous process has a thin apex with lower radiopharmaceutical uptake than the S2 spinous process in each pair of images. The color scale on the right of panel B represents radiopharmaceutical uptake (photon count range, 0 [black] to maximum count [145; white]) evident on each of the scintigraphic images.
Citation: Journal of the American Veterinary Medical Association 260, 1; 10.2460/javma.20.08.0428
Representative paired dorsal (top) and dorso-20°-caudal oblique (bottom) nuclear scintigraphic images of horses described in Figure 1, showing the scintigraphic types (type 1a [A], type 1b [B], type 2 [C], and type 3 [D]) described in Figure 2. In all images, the horse’s left side is toward the left and cranial is toward the top. Notice that the S1 spinous process has a thin apex with lower radiopharmaceutical uptake than the S2 spinous process in each pair of images. The color scale on the right of panel B represents radiopharmaceutical uptake (photon count range, 0 [black] to maximum count [145; white]) evident on each of the scintigraphic images.
Citation: Journal of the American Veterinary Medical Association 260, 1; 10.2460/javma.20.08.0428
Representative paired dorsal (top) and dorso-20°-caudal oblique (bottom) nuclear scintigraphic images of horses described in Figure 1, showing the scintigraphic types (type 1a [A], type 1b [B], type 2 [C], and type 3 [D]) described in Figure 2. In all images, the horse’s left side is toward the left and cranial is toward the top. Notice that the S1 spinous process has a thin apex with lower radiopharmaceutical uptake than the S2 spinous process in each pair of images. The color scale on the right of panel B represents radiopharmaceutical uptake (photon count range, 0 [black] to maximum count [145; white]) evident on each of the scintigraphic images.
Citation: Journal of the American Veterinary Medical Association 260, 1; 10.2460/javma.20.08.0428
Scintigraphic types 1a and 1b corresponded to the anatomic description of the LS articulation and divergent spinous processes.9,25 Horses were categorized as type 1a if they had 6 true lumbar vertebrae total between the caudalmost thoracic vertebra and S1 and their L6 spinous process angled cranially and was identified cranial to the tubera sacrale, making the distance between spinous processes shorter between L5 and L6 than between L6 and S1. In contrast, horses with type 1b anatomic variant had only 5 true lumbar vertebrae total, with or without a transitional L1 vertebra (ie, with 1 or 2 ribs). Similar to type 1a, the spinous process of the caudalmost lumbar vertebra in type 1b horses angled cranially and was identified cranial to the tubera sacrale, making the distance between the spinous processes shorter between the 2 most caudal lumbar vertebrae than between the caudalmost lumbar vertebra and S1.
Horses with scintigraphic type 2 anatomic variant had 6 true lumbar vertebrae total, and their L6 spinous process was identified in the cranial half of the space between both tubera sacrale (intersacral space), making the distance between spinous processes similar for L5 and L6 versus L6 and S1. Criteria for type 3 variant were 5 true lumbar vertebrae, LS synostosis (fusion of the L6 and S1 vertebral bodies), and L6 with spinous process angled caudally like a sacral vertebra, making the distance between spinous processes greater between L5 and L6 than between L6 and S1.
Particular attention was paid to identify whether ribs versus transverse processes were present adjacent to the vertebrae to differentiate between the caudalmost thoracic vertebra and L1 in each horse. For horses in which this distinction was not clear on the dorsal plane scintigraphic images, reviewers evaluated the lateral oblique images to facilitate identification of ribs versus transverse processes.
Transrectal ultrasonography
Acquisition of images
The day after undergoing nuclear scintigraphy, horses underwent transrectal ultrasonography, restrained in stocks and sedated with detomidine (6 to 12 μg/kg, IV) and butorphanol tartrate (10 to 20 μg/kg, IV). Transrectal ultrasonographic examinations were performed as previously described16,19,20,21 with a 5- to 7.5-MHz curvilinear transrectal transducer (Aloka-Hitachi; Hitachi Medical Systems SAS) operated by 1 of 3 senior veterinary specialists in equine locomotor pathology who were experienced in musculoskeletal ultrasonography of horses. All ultrasonographic examinations included at least median plane ultrasonographic images of the LS intervertebral symphysis.
Image interpretation
Ultrasonographic images for each horse were anonymized, and the order of horses evaluated was completely randomized by means of random permutation to avoid bias during examination of the images. Images were reviewed by 1 observer (GV) who was asked to classify horses according to a grading system (ultrasonographic grade 1, 2, or 3) on the basis of the craniocaudal width of the LS IVD (reference range,19 2 to 6 mm; Figure 4). Horses were assigned grade 1 if their LS IVD craniocaudal width was ≥ 2 and ≤ 6 mm at its dorsoventral midpoint, with or without visualization dorsally to the vertebral canal and spinal cord. Grade 2 was assigned to horses with either an LS IVD craniocaudal width < 2 mm at its dorsoventral midpoint, no visualization of the ventral aspect of the vertebral canal because of a dorsally narrow IVD space, or both. Grade 3 was assigned to horses with complete LS synostosis (fused vertebral bodies).
Representative ventrodorsal transrectal ultrasonographic images of the LS intervertebral symphysis in 3 of the 243 horses described in Figure 1 and acquired with a small curvilinear transducer on the median plane, showing characteristics of anatomic variants classified as ultrasonographic grade 1 (A), 2 (B), or 3 (C), with cranial toward the left and dorsal toward the top of each image. A—Grade 1 is characterized by a clinically normal intervertebral disc (IVD; 3) with a width ≥ 2 and ≤ 6 mm at its dorsoventral midpoint between the caudalmost lumbar vertebra (2) and S1 (1). Also evident are the ventral longitudinal ligament (4), dorsal longitudinal ligament (5), ventral wall of the dura mater (6), subarachnoid space (7) around the medullary cone of the spinal cord, and ligamentum flavum (interarcurate) (8). B—This horse has ultrasonographic grade 2, characterized with a thin (< 2-mm) IVD and partial dorsal synostosis between the caudalmost lumbar vertebra and S1 and no visualization dorsally to the vertebral canal and spinal cord. C—Grade 3 in this horse is evident with complete LS synostosis (fused vertebral bodies of the caudalmost lumbar vertebra and S1) and no LS IVD. 1 = S1. 2 = Caudalmost lumbar vertebra. 3 = LS IVD. 4 = Ventral longitudinal ligament. 5 = Dorsal longitudinal ligament. 6 = Ventral wall of the dura mater. 7 = Subarachnoid space around the medullary cone of the spinal cord. 8 = Ligamentum flavum (interarcurate).
Citation: Journal of the American Veterinary Medical Association 260, 1; 10.2460/javma.20.08.0428
Representative ventrodorsal transrectal ultrasonographic images of the LS intervertebral symphysis in 3 of the 243 horses described in Figure 1 and acquired with a small curvilinear transducer on the median plane, showing characteristics of anatomic variants classified as ultrasonographic grade 1 (A), 2 (B), or 3 (C), with cranial toward the left and dorsal toward the top of each image. A—Grade 1 is characterized by a clinically normal intervertebral disc (IVD; 3) with a width ≥ 2 and ≤ 6 mm at its dorsoventral midpoint between the caudalmost lumbar vertebra (2) and S1 (1). Also evident are the ventral longitudinal ligament (4), dorsal longitudinal ligament (5), ventral wall of the dura mater (6), subarachnoid space (7) around the medullary cone of the spinal cord, and ligamentum flavum (interarcurate) (8). B—This horse has ultrasonographic grade 2, characterized with a thin (< 2-mm) IVD and partial dorsal synostosis between the caudalmost lumbar vertebra and S1 and no visualization dorsally to the vertebral canal and spinal cord. C—Grade 3 in this horse is evident with complete LS synostosis (fused vertebral bodies of the caudalmost lumbar vertebra and S1) and no LS IVD. 1 = S1. 2 = Caudalmost lumbar vertebra. 3 = LS IVD. 4 = Ventral longitudinal ligament. 5 = Dorsal longitudinal ligament. 6 = Ventral wall of the dura mater. 7 = Subarachnoid space around the medullary cone of the spinal cord. 8 = Ligamentum flavum (interarcurate).
Citation: Journal of the American Veterinary Medical Association 260, 1; 10.2460/javma.20.08.0428
Representative ventrodorsal transrectal ultrasonographic images of the LS intervertebral symphysis in 3 of the 243 horses described in Figure 1 and acquired with a small curvilinear transducer on the median plane, showing characteristics of anatomic variants classified as ultrasonographic grade 1 (A), 2 (B), or 3 (C), with cranial toward the left and dorsal toward the top of each image. A—Grade 1 is characterized by a clinically normal intervertebral disc (IVD; 3) with a width ≥ 2 and ≤ 6 mm at its dorsoventral midpoint between the caudalmost lumbar vertebra (2) and S1 (1). Also evident are the ventral longitudinal ligament (4), dorsal longitudinal ligament (5), ventral wall of the dura mater (6), subarachnoid space (7) around the medullary cone of the spinal cord, and ligamentum flavum (interarcurate) (8). B—This horse has ultrasonographic grade 2, characterized with a thin (< 2-mm) IVD and partial dorsal synostosis between the caudalmost lumbar vertebra and S1 and no visualization dorsally to the vertebral canal and spinal cord. C—Grade 3 in this horse is evident with complete LS synostosis (fused vertebral bodies of the caudalmost lumbar vertebra and S1) and no LS IVD. 1 = S1. 2 = Caudalmost lumbar vertebra. 3 = LS IVD. 4 = Ventral longitudinal ligament. 5 = Dorsal longitudinal ligament. 6 = Ventral wall of the dura mater. 7 = Subarachnoid space around the medullary cone of the spinal cord. 8 = Ligamentum flavum (interarcurate).
Citation: Journal of the American Veterinary Medical Association 260, 1; 10.2460/javma.20.08.0428
Statistical analysis
Repeatability of nuclear scintigraphic evaluations
Observer 1 (GV) performed 2 rounds of evaluations of the scintigraphic images within 2 weeks of each other, and intraobserver reliability analysis was performed. Interobserver agreement was performed with results from the second round of evaluation performed by observer 1 and results from a single round of evaluation by observer 2 (FA). Intra- and interobserver reliability of scintigraphic image evaluation were determined with the kappa (κ) statistic and 95% CI for the κ value. Agreement was interpreted on the basis of the lower limit of the 95% CI for the κ value (< 0 = poor, between 0 and 0.20 = slight, between 0.21 and 0.40 = fair, between 0.41 and 0.60 = moderate, between 0.61 and 0.80 = good, and ≥ 0.81 = excellent).
Agreement between nuclear scintigraphic type and transrectal ultrasonographic grade
In the nuclear scintigraphic classification system used, the difference between types 1a and 1b depended on the number of lumbar vertebrae. In both types, the LS articulation was similar: the spinous process of the caudalmost lumbar vertebra angled cranially and was identified cranial to the tubera sacrale. Because transrectal ultrasonographic examinations focused on ventral aspects of the lumbar and LS regions of the vertebral column and did not provide visualization of the spinous processes to assess angulation, we considered anatomic variant types 1a and 1b together as type 1 for agreement analyses with the Cohen κ test to evaluate the agreement between results for assignments of scintigraphic type (1, 2, or 3) and ultrasonographic grade (1, 2, or 3).
Period prevalence of the anatomic variations
Data were collected in a spreadsheet for statistical analysis (XLSTAT Biomed version 2020.1.3; Addinsoft). Results for horses grouped on the basis of breed and sex were compared with χ2 tests for both imaging modalities. Values of P < 0.05 were considered significant. Numbers and percentages were reported. The associations between scintigraphic types or ultrasonographic grades and horse breed or sex were quantified by calculating ORs and 95% CIs for the ORs.
Results
Animals
There were 243 horses selected, which was just above the calculated minimum number of 239 horses needed to reach 80% power for statistical agreement tests. Examinations were conducted as a part of an overall physical examination or prepurchase examination (n = 113) or because of hind limb lameness (57), forelimb lameness or signs of neck stiffness (56), or signs of thoracolumbar stiffness (20), alone or in combination. Scintigraphic and transrectal ultrasonographic examinations of these horses had been performed at the discretion of the clinician or request of the referring veterinarian. As planned, there were 81 SFs, 81 FTs, and 81 TBs, among which each breed group consisted of 27 sexually intact females, 27 sexually intact males, and 27 geldings.
Repeatability of nuclear scintigraphic classification
Both observers classified scintigraphic type for each of the 243 horses. Results of the Cohen κ test for intra- and interobserver agreement were compiled (Table 1). Intraobserver repeatability was excellent (κ = 0.92; 95% CI, 0.88 to 0.96), with an overall agreement in 232 (95%) of 243 assignments of scintigraphic type. More specifically, in a binary analysis on the basis of assigned type, the reliability was excellent for types 1 (1a and 1b combined), 1a alone, 2, and 3. The agreement was good for the type 1b alone. Interobserver agreement was excellent (κ = 0.93; 95% CI, 0.90 to 0.97), with an overall agreement in 233 (96%) of 243 assignments of scintigraphic type. More specifically, the agreement was excellent for types 1 (1a and 1b combined), 1a alone, and 2 and was good for types 1b alone and 3.
Intraobserver (observer 1) and interobserver (observers 1 and 2) agreement of results for classification of the nuclear scintigraphic type (1a, 1b, 2, or 3) of lumbosacral (LS) articulation anatomic variant in 243 horses (81 Selle Français Warmbloods, 81 French Standardbred Trotters, and 81 Thoroughbreds) that underwent nuclear scintigraphy of the lumbar and sacral vertebrae and pelvis between January 2016 and December 2019.
| Agreement | κ Value (95% CI) | Agreement strength |
|---|---|---|
| Intraobserver | ||
| Overall | 0.92 (0.88–0.96) | Excellent |
| Type 1a alone | 0.94 (0.88–0.97) | Excellent |
| Type 1b alone | 0.82 (0.67–0.91) | Good |
| Type 1 (1a and 1b) | 0.92 (0.85–0.95) | Excellent |
| Type 2 | 0.95 (0.89–0.98) | Excellent |
| Type 3 | 0.94 (0.84–0.98) | Excellent |
| Interobserver | ||
| Overall | 0.93 (0.90–0.97) | Excellent |
| Type 1a alone | 0.97 (0.92–0.99) | Excellent |
| Type 1b alone | 0.88 (0.75–0.94) | Good |
| Type 1 (1a and 1b) | 0.93 (0.86–0.96) | Excellent |
| Type 2 | 0.97 (0.92–0.99) | Excellent |
| Type 3 | 0.86 (0.74–0.92) | Good |
Period prevalences of anatomic variants
Results of skeletal scintigraphy and transrectal ultrasonography were compiled (Table 2). Anatomic variations were identified in both skeletal scintigraphy and transrectal ultrasonography. Of the 243 horses included in the study, 132 (54.3%) were identified as type 1 on nuclear scintigraphy, with a cranially angled spinous process of the caudalmost lumbar vertebra and the number of true lumbar vertebrae totaling either 6 (type 1a; 104/243 [42.8%]) or 5 (type 1b; 28/243 [11.5%]). There were 74 (30.5%) of the 243 horses assigned scintigraphic type 2, with a vertical spinous process of L6 in the cranial half of the intersacral space. The remaining 37 (15.2%) horses were assigned scintigraphic type 3, with the L6 spinous process angled caudally and identified in the caudal half of the intersacral space. On the basis of transrectal ultrasonographic images, 146 (60.1%) of the 243 horses had an LS IVD craniocaudal width within reference limits (≥ 2 and ≤ 6 mm at its dorsoventral midpoint) and were assigned grade 1, 68 (28.0%) had a thin LS IVD width (< 2 mm) and were assigned grade 2, and only 29 (11.9%) had LS synostosis with no LS IVD and were assigned grade 3.
Distribution of nuclear scintigraphic types (1, 2, and 3) of LS articulation anatomic variants in the 243 horses described in Table 1, stratified by horses grouped on the basis of transrectal ultrasonographic grade (1, 2, or 3) of LS intervertebral symphysis anatomic variant.
| Nuclear scintigraphic type | Transrectal ultrasonographic grade | |||
|---|---|---|---|---|
| Grade 1 | Grade 2 | Grade 3 | Total | |
| Type 1 | 115 | 16 | 1 | 132 |
| Type 2 | 26 | 47 | 1 | 74 |
| Type 3 | 5 | 5 | 27 | 37 |
| Total | 146 | 68 | 29 | 243 |
Breed
Anatomic variations were identified in both imaging modalities for all 3 breeds studied; however, distribution of the various types differed significantly (P < 0.05) among horses grouped by breed (Table 3). More specifically, nuclear scintigraphic type 1 was most commonly identified across all 3 breeds. The period prevalence of scintigraphic type 1 was significantly (P < 0.05) higher for SFs (53/81 [65%]) versus FTs (37/81 [46%]), and the odds of scintigraphic type 1 were significantly (OR, 2.25; 95% CI, 1.20 to 4.22; P < 0.05) higher for SFs than for FTs. Scintigraphic type 2 was significantly (P < 0.05) more common among FTs (32/81 [40%]) than among TBs (20/81 [25%]), and the odds of type 2 were significantly (OR, 1.99; 95% CI, 1.02 to 3.88; P < 0.05) higher for FTs, compared with TBs. The period prevalence of scintigraphic type 3 was significantly (P < 0.05) higher in TBs (19/81 [23%]), compared with SFs (6/81 [7%]), for which the odds of scintigraphic type 3 were significantly (OR, 0.26; 95% CI, 0.10 to 0.67; P < 0.05) lower.
Distribution of nuclear scintigraphic types (1 [1a and 1b], 1a alone, 1b alone, 2, and 3) and transrectal ultrasonographic grades (1, 2, and 3) for the horses described in Table 1 grouped on the basis of breed and sex.
| Variable | No. of horses | No. (%) of horses per nuclear scintigraphic type | No. (%) of horses per transrectal ultrasonographic grade | ||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|
| 1 (1a and 1b) | 1a alone | 1b alone | 2 | 3 | 1 | 2 | 3 | ||||
| Breed | |||||||||||
| Selle Français Warmbloods | 81 | 53 (65) | 43 (53) | 10 (12) | 22 (27) | 6 (7) | 63 (78) | 12 (15) | 6 (7) | ||
| French Standardbred Trotters | 81 | 37 (46) | 34 (42) | 3 (4) | 32 (39) | 12 (15) | 42 (52) | 30 (37) | 9 (11) | ||
| Thoroughbreds | 81 | 42 (52) | 27 (33) | 15 (18) | 20 (25) | 19 (23) | 41 (51) | 26 (32) | 14 (17) | ||
| Sex | |||||||||||
| Females | 81 | 45 (56) | 38 (47) | 7 (9) | 20 (25) | 16 (20) | 48 (59) | 22 (27) | 11 (14) | ||
| Males | |||||||||||
| Sexually intact | 81 | 45 (56) | 34 (42) | 11 (14) | 26 (32) | 10 (12) | 52 (64) | 21 (26) | 8 (10) | ||
| Geldings | 81 | 42 (52) | 32 (39) | 10 (12) | 28 (35) | 11 (14) | 46 (57) | 25 (31) | 10 (12) | ||
| Total | 243 | 132 (54.3) | 104 (42.8) | 28 (11.5) | 74 (30.5) | 37 (15.2) | 146 (60.1) | 68 (28.0) | 29 (11.9) | ||
Similarly, ultrasonographic grade 1 LS intervertebral symphysis was most commonly identified across all 3 breeds (Table 3). The period prevalence of ultrasonographic grade 1 was significantly (P < 0.05) higher for SFs (63/81 [78%]), compared with FTs (42/81 [52%]) or TBs (41/81 [51%]), and the odds of grade 1 were greater for SFs, compared with FTs (OR, 3.25; 95% CI, 1.66 to 6.38; P < 0.05) or TBs (OR, 3.42; 95% CI, 1.74 to 6.70; P < 0.05). The period prevalence of ultrasonographic grade 2 was similar for FTs (30/81 [37%]) and TBs (26/81 [32%]), whereas the odds of grade 2 were significantly lower for SFs, compared with FTs (OR, 0.30; 95% CI, 0.14 to 0.63; P < 0.05) or TBs (OR, 0.37; 95% CI, 0.17 to 0.79; P < 0.05). The period prevalence of ultrasonographic type 3 did not differ substantially among the 3 breeds.
Sex
Anatomic variations were identified in both imaging modalities in sexually intact females, sexually intact males, and geldings (Table 3). The distribution of the various scintigraphic types and ultrasonographic grades did not differ substantially for horses grouped on the basis of sex.
Agreement between scintigraphic type and ultrasonographic grade
Most (115/132 [87.1%]) horses identified as scintigraphic type 1 were also classified as ultrasonographic grade 1 (Table 2). Similarly, most (47/74 [64%]) horses identified as type 2 on nuclear scintigraphy were also classified as ultrasonographic grade 2, and most (27/37 [73%]) horses classified as scintigraphic type 3 were also classified as ultrasonographic grade 3. The overall agreement between scintigraphic type and ultrasonographic grade was 77.8% (189/243) and judged moderate with a κ value of 0.61 (95% CI, 0.52 to 0.70). More specifically, agreement was good for the association between results for nuclear scintigraphic type 3 and ultrasonographic grade 3 (κ value = 0.79; 95% CI, 0.65 to 0.88) and moderate for the association between results for scintigraphic type 1 and ultrasonographic grade 1 (κ value = 0.60; 95% CI, 0.49 to 0.69) and between results for scintigraphic type 2 and ultrasonographic grade 2 (κ value = 0.52; 95% CI, 0.40 to 0.63).
Discussion
The present study described in vivo occurrence of LS anatomic variations in a large group of horses that comprised 3 breeds that predominate in France and are used in sports and racing activities. Descriptions were provided for the anatomic variants of the LS intervertebral symphysis graded on the basis of transrectal ultrasonographic findings and of the LS articulation, primarily focused on the angulation of the caudalmost lumbar spinous process, classified by type on the basis of nuclear scintigraphic findings. The hypothesis that the angulation of the spinous process of the caudalmost lumbar vertebra identified on nuclear scintigraphy would correspond with the LS symphysis anatomic variant identified on transrectal ultrasonography was not verified in the present retrospective study.
The system we developed to classify scintigraphic type (1a, 1b, 2, or 3) was easily used by both observers. Intraobserver repeatability (observer 1) and agreement between both observers for the scintigraphic types assigned were very good. However, the overall agreement (189/243 [77.8%]) between results for the scintigraphic type and transrectal ultrasonographic grade was moderate (κ = 0.61; 95% CI, 0.52 to 0.70).
Various frequencies of LS synostosis have been reported, and a study17 of 20 horses representing multiple breeds shows that LS synostosis was identified in 2 horses (1 Standardbred and 1 Swedish Warmblood). A study11 of 36 cadaveric TBs shows that LS synostosis was not identified among the group. Conversely, Stubbs et al12 reported that postmortem identification of LS synostosis occurred among 16 (25%) of 65 TBs, 0 of 24 Standardbreds, and 7 (23%) of 31 horses of other breeds. More recently, investigators described in vivo findings for transrectal ultrasonography of the LS intervertebral symphysis and reported that LS synostosis was identified in 0% (0/43)20 and 20% (13/64)6 of horses evaluated. Additionally, one of those studies6 shows that 9% (6/64) of the horses had a thinner LS IVD than normal. In the present study, anatomic variants of the LS intervertebral symphysis were identified in all 3 breeds evaluated, and the distribution of variants differed significantly among breeds. Although most horses had an LS intervertebral symphysis with characteristics consistent with usual anatomic descriptions (ultrasonographic grade 1), anatomic variants were often identified. Further, only 11.9% (29/243) of the horses in the present study had LS synostosis, which was relatively lower than reported in previous studies6,12 performed on multiple breeds. In the present study, LS synostosis was more frequently identified in TBs, consistent with findings by Stubbs et al.12 However, contrary to that study,12 in which no LS synostosis was identified in the Standardbred group, LS synostosis was identified in 11% (9/81) of the FTs in the present study.
Regarding variation in the angulation of the L6 spinous process, Haussler et al11 showed that among 36 cadaveric TBs the L6 spinous process angled cranially in 36% (13/36), vertically in 36% (13/36), and caudally in 28% (10/36). Stubbs et al12 reported similar results, with the L6 spinous process angled caudally in 25% (30/120) of the specimens, compared with cranial angulation of the last lumbar spinous process in the remaining specimens.
Variations of the LS articulation were also identified with transrectal ultrasonography and nuclear scintigraphy in each of the 3 sexes (sexually intact females, sexually intact males, or geldings) of horses in the present study, and there was no meaningful difference in the distribution of variants across the sexes. To have uniform groups, the same number of animals in each sex group was included, but it is unlikely that castration could modify the LS conformation that is established congenitally. Thus, males in general (81 sexually intact males and 81 geldings) were overrepresented in the present study, which was a weak point in the selection of the cases. However, the sex of affected animals is usually considered in retrospective studies focused on lesion occurrence, particularly when associated with variables for type and level of activity. That is why the sex of animals included should be taken into account in future investigations of the prevalence of LS anatomic variants in horses with signs of LS or sacroiliac pain. Some studies in humans26,27 and dogs28,29,30 show association between variations of the LS articulation and the development of lesions, with the potential for the absence of clinical signs in individuals with anatomic variations.31 In the present study, detailed characterization of individual LS conformation was provided on the basis of vertebral column features identified with 2 complementary diagnostic imaging modalities used to image standing horses. Our findings represent a preliminary step toward further assessments of relationships that may exist between these anatomic variants and LS pathological findings or performance. Indeed, LS anatomic variants have been described as abnormal findings, but a hypothesis of their pathological origin has not been clearly put forward and demonstrated. Acquired pathological changes of the LS articulation include mainly fractures of the L6 vertebral fossa or S1 vertebral head, degenerative changes of the LS IVD, and arthropathies of the intertransverse LS joints.18 Secondary variation of the LS angulation or LS ankylosis as a result of end-stage pathological changes was never observed in the authors’ clinical cases. Therefore, although anatomic variants of LS articulation described in the present study may predispose affected horses to pathological changes, the anatomic variants described represent conformational variations, and our results may help to differentiate between clinically normal individual variations and clinically important pathological findings and to consequently improve the diagnostic accuracy of their detection with nuclear scintigraphy and transrectal ultrasonography.
Results of the present study described the distribution frequency of LS anatomic variants in a French population of 243 horses (81 of each SF, FT, and TB breeds) and may not apply to the whole population of horses. Our findings indicated that the distribution of anatomic variants significantly differed among horses grouped on the basis of breed but not for horses grouped on the basis of sex. Nuclear scintigraphy was useful to assess location and angulation of the spinous processes in the LS area; however, because the agreement between scintigraphic type and ultrasonographic grade was moderate, our results suggested that nuclear scintigraphy had limited ability to identify LS intervertebral symphysis anatomic variants. Further research is needed to determine potential relationships between anatomic variants of the LS articulation described in the present study and LS and sacroiliac lesions, clinical signs, and athletic performance in horses.
Acknowledgments
Equipment and facilities were supported by the European Regional Development Fund, Normandy region, Calvados County Council, Eperon Funds, and French Ministry of Agriculture and Research.
The authors declare that there were no conflicts of interest.
The authors thank Professor Loïc Desquilbet for his contribution to statistical analysis performed in this study.
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