Sidewinder gait in horses

Abstract Background Sidewinder gait in horses is poorly understood and characterized by walking with the trunk and pelvic limbs drifting to 1 side. Hypothesis/objectives To report causes, clinical and diagnostic features. Animals Horses examined at 2 institutions. Materials and Methods Retrospective study (2000‐2019). Cases with sidewinder gait, neurological and orthopedic examination, and diagnostic work up or postmortem evaluation were included. Descriptive statistics were performed. Results Twenty‐four horses (mean age 18.9 years) of various breeds and both sexes were included. Onset was acute (N = 10), subacute (N = 6), and insidious (N = 8). Electromyography and muscle biopsy supported neurologic disease and further aided in localizing site of lesion (N = 9/9). Neurologic causes included dynamic thoracolumbar spinal cord compression (N = 5), equine protozoal myeloencephalitis (N = 4, confirmed and presumed [2 each]), thoracic myelopathy of unknown etiology (N = 4), gliosis (N = 2), and thrombosis of thoracic spinal cord segments (N = 1). Non‐neurologic causes included osteoarthritis of the coxofemoral joint (N = 4), multiple displaced pelvic fractures (N = 2), bilateral rupture of the ligamentum capitis ossis femoris (N = 1), and severe myonecrosis of multiple pelvic limb muscles (N = 1). Case fatality was 79%. Conclusion and Clinical Importance Sidewinder gait is usually observed in older horses and can have neurologic or musculoskeletal etiologies. Electromyography can be used as a diagnostic aid to determine neurologic versus non‐neurologic disease and further localize those of neurologic origin. The condition often has a poor prognosis for function and life.


| INTRODUCTION
Sidewinder is a lay term used to describe horses with an unusual gait characterized by a disjointed movement of the thoracic and pelvic limbs, in which the trunk, pelvis, and pelvic limbs drift to 1 side while the thoracic limbs are usually normal. 1 In severe cases, horses spin or circle in 1 place with their pelvic limbs moving in 1 direction while the thoracic limbs move in a compensatory manner. Other common names used for this gait include side walker and crab walker. 1 The authors hypothesized that sidewinder gait has various etiologies including musculoskeletal, neurologic, or a combination of conditions resulting in this complex gait.

| MATERIALS AND METHODS
The cases consisted of horses seen at the William R. Pritchard Veterinary Medical Teaching Hospital (VMTH) from the University of California at Davis, the Centre for Equine Studies, Animal Health Trust (AHT) at Newmarket, and external consultation from equine private practices from 2000 to 2019. The electronic medical records of the VMTH and the AHT were searched using the words sidewinder, side walker, crab walker, pelvic sway, drifting, leaning, pivoting, T3-L3 myelopathy, T3-caudal myelopathy, and lumbosacral (LS). The nomenclature of T3 or L3, for example, refers to spinal cord segments and caudal means spinal cord caudal to those spinal cord segments. Three main criteria had to be met to be included in the study: (1) horses presenting with a sidewinder gait; (2) having a full physical, orthopedic, and neurological examination; and (3) having a diagnostic work up or a postmortem evaluation. Sidewinder gait was defined as horses walking with their trunk, pelvis, and pelvic limbs drifting or leaning to 1 side while walking. 1,2 In severe cases, horses spin or circle with their pelvic limbs while their thoracic limbs move in a compensatory way. 2 Horses with additional thoracic limb involvement were also included. Data retrieved from the medical record included signalment, history (onset, duration, progression), body posture (leaning, drifting, pivoting, dog sitting), posture of thoracic and pelvic limbs (limbs positioned in same or opposite direction), reluctance to move, stiffness, stilted gait, lameness and grade (American Association of Equine Practitioners [AAEP website, January 7, 2020 3 ], see below), and apparent pain upon palpation. Onset of sidewinder gait was defined as acute (<48 hours), subacute (48 hours to 1 week), and insidious (>1 week). The neuroanatomical localization and severity of signs were recorded for horses classified as neurologically abnormal. Diagnostic data included hematology and biochemistry panel, and imaging modalities such as radiography, ultrasonography, nuclear scintigraphy, or computed tomography. Prospectively from 2012, additional diagnostic tests included intra-articular anesthesia, electromyography (EMG), cerebrospinal fluid (CSF) analysis, and muscle biopsy. Not all diagnostics were performed in all cases. Treatment and outcome were also recorded.
Short-term survival was defined as survival to discharge. Of the horses discharged, follow-up was completed by use of medical records or telephone conversation with the owner. Postmortem evaluation was recorded when available.

| Lameness grading system
The grading system according to the AAEP guidelines 3 consisted of 6 grades from 0 to 5 as follows. Grade 0 consisted of a lameness not perceptible under any circumstances; grade 1 difficult to observe and not consistently apparent regardless of circumstances; grade 2 difficult to observe at a walk or when trotting in a straight line but consistently apparent under certain circumstances; grade 3 lameness consistently observable at a trot under all circumstances; grade 4 lameness obvious at a walk; and grade 5 lameness with minimal weight bearing in motion, rest or both.

| Neurological grading system
In brief, a modified grading system for signs of neurologic disease (eg, ataxia, proprioceptive dysfunction) as described by Lunn

| Perineural and intra-articular anesthesia
Perineural anesthesia of the tibial and fibular nerves, intra-articular anesthesia of the 3 compartments of the stifle, and intra-articular anesthesia of the coxofemoral joint were performed for all 4 horses seen at the AHT. A variable combination of nerve blocks was performed at the discretion of the attending clinician based on examination findings in the horses with suspected musculoskeletal disease seen at the VMTH.

| Electromyography
Electromyography was performed using a Nicolet (Nicolet Viasys Healthcare Model, Viking Quest, Madison, Wisconsin). A concentric needle electrode (26G by 50 mm length, recording area of 0.07 mm 2 ) was used to perform the EMG. A subdermal needle electrode (30G by 20 mm, Natus, F-E2-24 Genuine Grass Reusable Platinum Subdermal Needle Electrodes, 24 00 wire) was used as a ground and placed close to the area of examination. The area of EMG examination was based on the neuroanatomical localization.
Also, depending on ease of examination because of constant body leaning; other areas that were considered normal based on neurological examination were examined to confirm lack of abnormalities. When possible, the muscles examined bilaterally included the splenius, trapezius, supraspinatus, infraspinatus, triceps brachii, longissimus (cervis, thoracicus, and lumbaris), multifidus (thoracicus and lumbaris), iliocostalis, and gluteus medius. At least 5 sites per muscle were examined. Abnormal EMG was determined if decreased, prolonged, or absent insertional activity, and abnormal spontaneous activity such as fibrillation potentials (FP), positive sharp waves (PSW), complex repetitive discharges, and myotonic discharges were observed. The scoring system for EMG abnormalities was based on that used in human EMG as described by Kimura. 6 In brief, 5 different areas of each muscle selected were examined and EMG findings were assigned grades 0 to 4 based on the following.

| Histochemical evaluation of skeletal muscle
Muscle biopsies were collected for further investigation of possible cause(s) and definition of muscle atrophy as neurogenic versus disuse atrophy. Biopsies were collected from affected muscles according to EMG findings and other muscles at the discretion of the attending clinician. Lidocaine hydrochloride (1.5 mL) was applied SC as a local anesthetic. The method of collection included incisional or punch biopsy for superficial muscles and Bergstrom needle biopsy (AgnTho's AB, Lidingo, Sweden) for deeper muscles. Immediately after collection, the specimens were flash frozen in isopentane pre-cooled in liquid nitrogen and stored at −80 C until further processing. The following stains and reactions were performed: hematoxylin and eosin, modified Gomori trichrome, periodic acid Schiff, phosphorylase, esterase, Streptococcal protein G-horseradish peroxidase, ATPase at pH 9.8, 4.6, and 4.3, nicotinamide adenine dinucleotide, succinic dehydrogenase, acid phosphatase, alkaline phosphatase, and oil red O. Neurogenic muscle atrophy was defined by the presence of severe angular muscle atrophy of both fiber types (types 1 and 2).
Disuse atrophy was identified based on the presence of type 2 myofiber anguloid atrophy.

| Statistical analysis
Descriptive statistics were used in this study when applicable. Parametric data were presented as mean and SD, and nonparametric data as median and range.

| Physical examination and gait evaluation
Physiological variables were within reference range and no abnormalities other than the abnormal posture and gait were found upon physical examination. There was an apparent resistance or inability to pick up the pelvic limbs from the ground more profound in the limb supporting most of the weight in all horses. Fourteen horses appeared stiff and painful upon palpation of musculature and manipulation of the thoracolumbar (N = 7), pelvic (N = 4, bones), and coxofemoral joint (N = 3, 2 of which also had audible crepitus) areas. Fourteen horses had trouble laying down, and 7 had difficulty eating due to constant leaning and spinning to 1 side unless supported by a wall or fence ( Figure 1). Thoracic limb involvement was to a lesser grade (2 grades difference) than pelvic limbs according to a modified published grading system. 4 Horses with pelvic limb ataxia were graded as 4 of 5 (N = 13) and 3 of 5 (N = 3). Pelvic limb placement for all 16 horses was consistently irregular.

| Neurological and orthopedic evaluation
Eight horses were determined to have primary musculoskeletal disease. Seven horses demonstrated a grade 4 of 5 lameness and were consistently walking side ways to 1 side. The 8 horses varied between grades 4 and 5 lameness. Abnormal placement of their pelvic limbs was consistently regular.

| Intra-articular anesthesia of the coxofemoral joint
After negative responses to distal limb perineural anesthetic blocks, intra-articular anesthesia of the coxofemoral joint was performed in 4 horses seen at the AHT using 20 mL of mepivacaine. Synovial fluid was retrieved in all horses. Horses were assessed up to 1 hour after injection, but there was little alteration in gait. These horses were later diagnosed with severe coxofemoral arthritis (next sections).

| Histochemical evaluation of skeletal muscle
After EMG examination, muscle biopsies were collected in 9 horses

| Therapy
Horses with signs of neurologic disease were treated with non-steroidal anti-inflammatory drugs (NSAIDs, N = 11), antioxidants (vitamin E N = 7, and C N = 4), antiprotozoals (ponazuril, N = 3), and intravenous fluids (N = 6). Posture improved slightly in 4 horses that received NSAIDs, 2 that received ponazuril but sidewinder gait remained. Four horses with musculoskeletal disease were treated with NSAIDs ranging from a few days to weeks. Initial mild improvement of the posture, apparent pain, and sidewinder gait was noted within a few days but severity of signs recurred while on treatment. Two horses with osteoarthritis of the coxofemoral joint received intraarticular medication with methyl prednisolone acetate, but failed to respond.

| Outcome
Nineteen of 24 horses were euthanized (neurologic N = 12, nonneurologic N = 7). Six horses were discharged alive (neurologic N = 5, F I G U R E 2 Clinical presentation: musculature. Note musculature of pelvic area and pelvic limbs in 2 horses with acute onset of sidewinder gait. Images taken weeks after onset: A,B = neurologic disease; C = musculoskeletal disease non-neurologic N = 1). Two horses with presumed EPM were discharged home on a 90-day course of ponazuril (5 mg/kg orally once a day) and improved body posture, muscle mass, and 1 to 2 grades of ataxia and neurological deficits, but the sidewinder gait remained on follow-up visits (Figure 4). One of these 2 horses was euthanized at home for a combined fatality rate of 79%. A followup telephone call in the 5 remaining horses revealed no return to physical activity. Long-term follow-up (3 years) was available for 2 horses which were turned out in pasture with an improved but persistent sidewinder gait.   shown in this study. 9 Three horses had an AO CSF cytology and protein within reference range whereas those from LS CSF were abnormal. These 3 horses had vascular disease in thoracic spinal cord segments, thoracic compressive myelopathy, and presumed EPM with profound involvement of T3 to caudal spinal cord segments, each.

| Definitive diagnosis
Different spinal cord diseases can affect a variety of specific tracts, sensory, or motor neurons, or all, depending of the site of injury. Sensory spinal cord deficits present as ataxia, abnormal proprioception and altered sensory input; whereas motor deficits manifest as paresis or paralysis, dysmetrias, and weakness. 10 For instance, neuroaxonal dystrophy affects primarily sensory tracts and nuclei versus equine motor neuron disease affects lower motor neurons. 11,12 Compressive myelopathies regardless of cause (eg, cervical vertebral malformation, intervertebral disc disease, synovial cyst, mass-occupying lesions such as neoplasia) affect both sensory and motor tracts. Both, sensory and motor deficits were noted in the horses of the current study. However, the motor tracts (ventromedial and lateral) were more profoundly affected causing paraparesis, bilateral dysmetria, severe weakness, and walking drifting and leaning ipsilateral to the most affected side in these horses.
Equine protozoal myeloencephalitis has been suspected to cause sidewinder gait but not reported nor confirmed. 1 Here, we report 2 confirmed cases of EPM based on histopathological and molecular evaluation as the cause of the abnormal gait and posture. These 2 horses ages were 12 and 25 years of age. This disease more commonly affects horses younger than 4 years of age, whereas only 19.8% of cases are older than 8 years of age. [13][14][15] Of interest, 1 of these 2 horses had negative IFA titers for S neurona and N hughesi on both, serum and CSF. This horse developed acute severe neurological deficits and presented to our hospital 4 days later. It is possible that an immune response was not fully developed at the time of testing due to its acute and severe course. This horse had severe necrotizing lymphocytic, histiocytic, and eosinophilic myelitis with malacia of several thoracic spinal cord segments. The second confirmed horse had a large number of S neurona schizonts and severe mononuclear perivascular inflammation in the thalamus and substantia nigra with no evidence of spinal cord involvement. The thalamus is a major relay motor center of the brain and the substantia nigra is an important part of the basal nuclei which control motor function. 10  The case with a thrombus involving T14 to T15 spinal cord segments was unusual in its presentation (ambulatory, grade 4 of 5) despite having 70% involvement of the spinal cord compromising sensory and motor tracts and nuclei at that location. This horse displayed both motor (paraparesis, dysmetria, weakness) and sensory (ataxia, abnormal proprioception, apparent focal hyperesthesia of thoracic region) deficits of the pelvic limbs. Vascular injuries of the spinal cord such as ischemic and hemorrhagic myelopathies and vasculitis have been described in horses. [16][17][18][19][20][21] Ischemic myelopathies are uncommonly reported in young horses usually resulting from fibrocartilaginous embolism at the C6 to T1 spinal cord segments and presumed to be from extruded nucleus pulposus which was not evident in these cases. 16,17,21 Hemorrhagic myelopathies resulting in myelomalacia, inability to rise, and loss of pain perception are uncommon causes of severe neurological signs usually in young horses undergoing anesthesia for relatively short periods of time. [18][19][20] Herpes myeloencephalopathy caused by equine herpesvirus 1 (EHV-1) is a common cause of vasculitis, thrombosis, and hemorrhage of the spinal cord in horses. 22 However, due to onset, long duration with slow progression of abnormal gait in the horses from this report, EHV-1 infection was unlikely the cause of disease. Furthermore, horses with acute onset of neurological signs tested negative for EHV-1 infection.
Electromyography was used in this study (9 of 24 horses) because it is a simple, easy, and minimally invasive diagnostic technique that aids in the detection of disease processes that affect the electrical activity of the muscle. 6,23 Although EMG does not provide a definitive diagnosis, its alterations can support a clinical diagnosis. 23 The distribution of EMG abnormalities can assist in the localization of lesions to spinal cord segments, nerve plexuses, nerves, and muscles. 6 EMG in this study helped in further localization of lesions within suspected spinal cord segments (eg, narrowing the clinical localization from T3 to caudal myelopathy to specific spinal cord segments) identified upon neurological examination in all horses tested. Multifocal abnormal spontaneous activity was identified in multiple spinal cord segments in a horse with EPM, 4 horses with thoracic and lumbar compressive myelopathy, T14 to T15 in a horse with vascular injury, and T13 in a horse with focal gliosis. Two additional horses had multifocal EMG abnormalities which cause remained unknown. EMG was not done in the remaining horses due to safety concerns.
Ultrasonographic examination was only possible in 6 horses due to the degree and exacerbation of leaning with sedation, and it was useful for the detection of multiple pelvic fractures in 2 horses with recent trauma, and intervertebral disc disease in 2 horses. Intervertebral disc disease could be an incidental finding since it has been observed in clinically normal horses. 24,25 However, in some cases it could be clinically relevant as a cause of nerve root pain, extradural compressive myelopathy, and more uncommonly fibrocartilaginous embolism, or both. 17,24,26,27 Characterization of pelvic fractures is essential for determination of prognosis. 28 Ultrasonographic evaluation of the pelvis includes the coxofemoral joints, sacroiliac joints, and pubic symphysis and can be performed SC and transrectally in the standing horse. [28][29][30][31] Similar to the 1 case here, prognosis for multiple pelvic fractures particularly involving the acetabulum have the worst prognosis for returning to athletic performance. 28 In 1 horse with multiple pelvic fractures from this report, severe sidewinder gait improved over a year but did not completely resolve. It is of interest that sidewinder gait was not reported in 2 studies of 75 and 86 horses with pelvic fractures. 28,32 The contribution of pelvic fractures to sidewinder gait in the horses from this report was not fully investigated since a postmortem evaluation was not performed.
The sidewinder gait was also observed in association with apparent musculoskeletal pain and exclusion of other potential causes as previously described. 2 Bilateral degeneration of the articular cartilage of both the acetabulum and femoral head, and partial rupture of the left ligamentum capitis ossis femoris caused a sidewinder gait to the right in a 25-year old Welsh Cob stallion. 2 One horse from this report had bilateral coxofemoral luxation as the result of ligamentum capitis ossis femoris rupture with bilateral severe chronic osteoarthrosis causing leaning and side walking contralateral to the side with the more severe abnormalities; perhaps due to the inability to support weight on the most affected side as the result of complete luxation. However, a sidewinder gait was not reported in a study of 7 horses with coxofemoral subluxation presented with severe acute lameness (N = 6 grade 4 of 5, N = 1 grade 3 of 5) in which diagnosis was confirmed using ultrasonography. 33 The diagnosis of coxofemoral subluxation required dynamic visualization of the femoral head being displaced from the acetabulum while placing weight on the affected limb and replacement into its normal position upon resting the limb. 33 Acetabular rim fractures were also visualized in 6 of 7 horses; all had a poor outcome and 4 were euthanized. 33 A postmortem evaluation performed in 2 of those horses showed elongation but intact ligamentum capitis ossis femoris. 33 Furthermore, 5 horses in the current series had severe osteoarthritis of the coxofemoral joint which was confirmed radiographically in 4 and at postmortem evaluation in all horses. Radiographs were acquired with the horses standing as described (lateral dorsal 30 to lateral ventral oblique images) and also in dorsal recumbency under general anesthesia. 34 The images acquired standing confirmed the presence of periarticular new bone, but much more detailed information about joint congruity, the extent of periarticular modeling and subchondral bone pathology was acquired from the images obtained under general anesthesia. The clinical relevance of the radiological abnormalities was supported by the presence of audible crepitus during passive manipulation of the coxofemoral joint in 2 horses and the results of ultrasonography in 2 other horses. A previous study demonstrated a similar ability to diagnose the presence of osteoarthritis of the coxofemoral joint using either radiography performed in standing horses or percutaneous ultrasonography. 35 Intra-articular anesthesia of the coxofemoral joint did not improve the gait in the horses from this report. Failure to improve is likely to be related to subchondral bone pain as observed in other joints. 36 The cause of severe diffuse myonecrosis of muscles of the pelvis and pelvic limbs in 1 horse remained undetermined. Trendelenburg syndrome in humans results in hip abductor weakness and can have various etiologies. 37 The gluteus medius and profundus are unilaterally weak and damaged resulting in the inability to maintain the pelvis in a normal position; therefore dropping the pelvis ipsilaterally and leaning when walking to the contralateral side. 37 It is unclear here if something similar occurred to this horse. Treatment in these horses was mainly supportive and palliative to address possible pain and inflammation, oxidative damage, and in some cases specific such as the use of antiprotozoal medication for those horses with presumed EPM. Although short-term improvement was observed with therapy, the sidewinder gait remained unresolved. The fatality rate in this study was 79% (N = 19 of 24). Resuming previous physical activity was not achieved in the remaining live horses and long-term follow-up in 2 horses out in pasture revealed a persistent sidewinder gait.
In conclusion, sidewinder gait can have a variety of causes involving a neurologic, musculoskeletal, or both etiologies. Sidewinder gait is more commonly seen in older mature horses of any breed and sex. Sidewinders represent a diagnostic challenge due to excessive leaning, often constant spinning, instability while standing, and exacerbation of signs with sedation that might be needed to pursue diagnostics. The side of leaning might be ipsilateral or contralateral to the side of the injury depending on underlying cause, anatomical region, and severity. It appears from this small group of horses that prognosis for recovery of function is grave and poor for life. Electromyography proved to be useful to further localize lesions and aid in the determination of neurologic versus orthopedic causes. A major limitation of this study was the low number of cases with a definitive etiology. Furthermore, a cause and effect for the abnormal gait based on clinical and limited diagnostic findings in all the remaining horses was not proven.

ACKNOWLEDGMENT
The authors thank the clinicians and pathologists involved with the cases.