Peripheral neuropathy is an uncommon cause of forelimb lameness in horses.1 This condition can involve the nerve roots of the brachial plexus, the brachial plexus itself, or nerves arising from it. The ventral roots from the sixth to the eighth cervical nerves and from the first and second thoracic nerves converge between the scalene muscles and the medial aspect of the shoulder to form the brachial plexus in the axillary space.2–5 Nerves arising from the brachial plexus include the suprascapular nerve (innervating the supraspinatus and infraspinatus muscles), axillary nerve (innervating the deltoideus, teres minor, and cleidobrachialis muscles), radial nerve (innervating the extensor muscles of the elbow joint, carpus, and digit), musculocutaneous nerve (innervating the flexor muscles of the elbow joint), and the median and ulnar nerves (innervating the caudal antebrachial flexor muscles).2–5 Trauma (including pressure, stretching, and transection) is the most frequent cause of peripheral neuropathy of a forelimb.6 Nerve lesions resulting from mechanical trauma have been classified into 3 categories according to the degree of damage to a single nerve fascicle: neurapraxia results from mild compression of the fascicle without morphological change of the axon, axonotmesis is caused by crushing with damage to the axon and preservation of the myelin sheath, and neurotmesis results from severing of the entire fascicle (axon and myelin sheath).6–10
Compression between the scapula and the ribs has been considered as the most common cause of injury to the brachial plexus or to the proximal part of the nerves emanating from the plexus.10,11 The suprascapular nerve is mainly susceptible to injury in the region where it crosses the thin cranial border of the scapula.6,7,10,12–17 Local subclinical neuropathy at this level, even in apparently healthy horses, can increase fragility of the nerve and its susceptibility to injury when the limb is suddenly thrust backward.7,18 Clinical signs of suprascapular nerve injury include subsequent neurogenic atrophy of the supraspinatus and infraspinatus muscles and, in most cases, lateral instability of the shoulder during the stance phase of the gait.6,7,9,10,12–17 Instability of the shoulder (commonly called sweeny) has also been reported secondary to lesions of the brachial plexus or of the ventral roots of its contributing nerves.19 Radial nerve fibers can be overstretched during hyperextension of the limb in a backward direction or in extreme abduction of the shoulder18,20; the nerve can also be compressed during general anesthesia of horses positioned in lateral recumbency,11,20,21 and it can be torn or compressed by trauma to the humerus or the elbow joint.9,11 The clinical signs of radial nerve injury depend on the severity, extent, and nature of the lesion as well as the site or sites of damage, and range from distal displacement of the olecranon tuberosity (ie, dropped elbow sign) and complete inability to stand on the affected limb to a slight tendency to stumble.1,6,9,11,19,20,22 Injury to the musculocutaneous nerve is rare and results in atrophy of the biceps brachii and brachialis muscles; typically, no clinically relevant gait abnormality is observed in affected horses.1,6,9,11 The median and ulnar nerves can be injured by direct external trauma or following a humeral fracture,6,9 with signs including hyperextension of the distal aspect of the affected limb and a somewhat stiff gait, but the effect on locomotion is moderate because the stay apparatus of the forelimb and the numerous intramuscular aponeuroses in the caudal antebrachial muscles partly compensate for the neurologic impairment.2–5
Although the literature includes several reports7,10,12,14–16,22,23 of horses with peripheral neuropathy of forelimbs, to our knowledge, no retrospective study of these injuries in a large number of horses has been published. Therefore, the purpose of the study reported here was to determine the clinical, radiographic, and ultrasonographic findings and outcomes of horses with peripheral neuropathy of a forelimb.
Materials and Methods
Case selection
Medical records of horses admitted to the Center of Imaging and Research on the Equine Locomotor Affections or to the Equine Clinic of the Ecole Nationale Vétérinaire d'Alfort, France, between January 1, 2000, and December 31, 2013, were reviewed. Horses with a diagnosis of a neurologic deficit of a forelimb determined on the basis of clinical (physical and dynamic) examination findings were included in the study.
Horses with acute and severe lameness were excluded if another lesion of the same limb (eg, a fracture) contributed to the clinical signs. Horses with peripheral neuropathy that developed subsequent to general anesthesia were also excluded.
Medical records review
Data obtained from the records included age, breed, sex, use, history, results of physical and lameness examinations, diagnostic imaging methods and results, treatments, management, and outcomes. Horses were grouped as having 1 of 3 types of predominant nerve injury on the basis of clinical signs (including localization of amyotrophy) and the results of diagnostic imaging procedures. These included suprascapular nerve injury, axillary nerve injury, or radial nerve injury, alone or in association with damage to other nerves.
Examination protocol
Muscle atrophy was subjectively graded on the basis of comparison of muscle body volume between affected and contralateral forelimbs and was designated as mild (discrete asymmetry of the muscle body volume), moderate (clear asymmetry and reduction of the muscle body volume), marked (obvious asymmetry with flattening of muscle body), or severe (extreme asymmetry with prominence of the bony structures). Lameness examination was performed for each horse and recorded on videotape. The grade of lameness was established in accordance with the lameness scale of the American Association of Equine Practitioners24 (0 = no lameness is perceptible under any circumstances; 1 = lameness is difficult to observe and is not consistently apparent, regardless of circumstances [eg, under saddle, circling, or on an incline or hard surface]; 2 = lameness is difficult to observe at a walk or when trotting in a straight line but consistently apparent under certain circumstances [eg, weight-carrying, circling, or on an incline or hard surface]; 3 = lameness is consistently observable at a trot under all circumstances; 4 = lameness is obvious at a walk; or 5 = lameness produces minimal weight bearing in motion or at rest or results in complete inability to move). Diagnosis of suprascapular nerve injury was made on the basis of shoulder joint instability and infraspinatus and supraspinatus muscle atrophy. Diagnosis of axillary nerve injury was made on the basis of specific atrophy of the deltoideus muscle, cleidobrachialis muscle, or both.3 Radial nerve paralysis was diagnosed when a dropped elbow sign was present, there was a clear extension deficit of the carpus and distal joints, or both. Other nerve injuries were diagnosed on the basis of specific muscle atrophy or loss of sensory perception as described elsewhere.3
Radiographic and ultrasonographic examinations were performed for all horses. The regions examined were determined on the basis of clinical signs and results of physical examination for each animal. Radiographic examination of the affected limb included ≥ 1 of the following: mediolateral images of the scapulohumeral joint, mediolateral and craniocaudal images of the elbow joint, a mediolateral image of the humerus, and left-to-right lateral-lateral images of the cervical spine (with views including T1 and T2). Ultrasonographic examination included the scapular area (affected and unaffected), shoulder joint, brachium, elbow joint, antebrachium, cervical spine, or a combination of these. The lateral aspects of elbow joints were examined by use of a 7.5-MHz linear transducer with a standoff pad, and other areas were scanned with a 5.5-MHz convex transducer.
Management of horses and outcome assessment
Management was conservative and generally consisted of a period of stall or box rest (ranging from 2 weeks to 1 year) followed by hand walking, turnout in a small paddock, and progressive return to exercise (being ridden or driven). Horses that were in training at the time of examination and were considered sound enough to work had training activities continued. Systemic administration of drugs and other complementary treatments varied; these were determined by the attending clinician in consultation with the client, and relevant information was collected from medical records. Treatments (given alone or in combination) included systemic administration of anti-inflammatory drugs, ultrasound-guided local injection of a nanopolysaccharide (regenerating agent) solution,25 mesotherapy,26 and electrostimulation27 as described elsewhere, as well as physiotherapy and homeopathic treatment.
Long-term follow-up information was collected ≥ 9 months after the initial consultation, and was obtained by reexamination of horses or by telephone communication with owners and referring veterinarians when reexamination could not be performed. Recovery time was calculated from the time of onset of clinical signs to the time that the horse was allowed to engage in its previous activities or intended use. Adult horses (defined as horses of an age to be used in their intended sport or racing activities) were considered to have a positive outcome if they returned to athletic soundness or to their previous level of athletic activity, and juvenile horses (defined as horses too young to perform in their intended sport or racing activities) were considered to have a positive outcome if they were deemed sound enough to begin a training program. Outcome was considered negative when an adult horse could not be returned to its previous use, a juvenile horse was not sound enough to enter a training program, or any horse was euthanized because of the nerve injury.
Results
Twenty-seven horses met the criteria for inclusion in the study. The predominant injury was to a suprascapular nerve in 11 horses, an axillary nerve in 2 horses, and a radial nerve (alone or in combination with injury to associated nerves) in 14 horses.
Suprascapular nerve injuries
Horses grouped as having suprascapular nerve injuries included 6 mares or fillies, 3 stallions or colts, and 2 geldings. Breeds or breed types included Thoroughbred (n = 7), French Trotter (2), and warmblood (2). The mean age was 3.7 years (median, 3; range, 11 months to 8 years). Adult horses were used for racing (n = 5 [3 Thoroughbreds and 2 French Trotters]), show jumping (1), dressage (1), and breeding (1). Four horses were referred for evaluation because of instability of the shoulder joint (≤ 2 months' duration in 2 horses and > 6 months' duration in the remaining 2). Four horses were examined because of muscle atrophy in the shoulder region (≤ 1 month's duration in 2 horses and 2 months' duration in 2). Three horses were examined because of forelimb lameness of ≤ 2 months' duration.
Three horses had a known history of trauma in the field or during competition, and trauma was suspected in 4 horses. The cause of injury was unknown for the other 4 horses. The right forelimb was affected in 6 horses, and the left was affected in 5. After the onset of injury, 2 horses were reportedly non–weight bearing on the affected limb and 5 were markedly lame at a walk. Atrophy of the supraspinatus muscle, infraspinatus muscle, or both had been identified in 7 horses by the referring practitioner ≤ 14 days after injury. No information from the initial examination was available for the other 4 horses. Four horses were described as having a marked improvement in lameness grade after ≤ 1 month of rest and rehabilitation following the initial examination (prior to the referral visit); all of these horses had received NSAIDs. No data on medical treatment or improvement after the initial evaluation were available for the other 7 horses. The mean duration of clinical signs prior to referral was 75 days (median, 60 days; range, 17 to 240 days).
At the time of the referral examination at the study facility, atrophy of the supraspinatus muscle, infraspinatus muscle, or both was present in all horses (severe in 6, marked in 3, and moderate in 2). Other findings included weakness in resisting manual retraction of the affected limb (n = 2), instability of the shoulder while standing (1), thickening of the point of the shoulder (1), and abnormal retraction and abduction of the limb while standing (1).
All 11 horses had instability of the affected shoulder joint (with lateral deviation) at a walk. When examined trotting in a straight line, 5 horses had grade 3 lameness, 2 had grade 1 lameness, and 4 had a lameness grade of 0 (ie, were sound). Five horses had a markedly reduced cranial phase of the step of the affected limb, compared with that of the contralateral limb.
Radiographic examination included views of the affected shoulder joint (n = 11 horses), elbow joint (7), humerus (1), and cervical spine (8). Radiographic findings included mild scapulohumeral dysplasia with discrete periarticular bone remodeling (n = 2) and mild osteoarthrosis of C6-7 (4); none of these findings were considered clinically relevant. The shoulder area was examined ultrasonographically in all 11 horses; 10 horses had ≥ 2 abnormalities detected, and 1 horse had 1 abnormality detected. Findings included atrophy of the supraspinatus muscle, infraspinatus muscle, or both (11 horses, including 7 with severe atrophy of 1 or both muscles; Figure 1); synovial effusion of the scapulohumeral joint (8 horses, including 4 with marked to severe synovial effusion, hypertrophy of the synovial membrane and villi, or intrasynovial echogenic floating spots [or some combination of these]); and synovial effusion of the bicipital bursa (4 horses). Other findings included osteoarthrosis of C6-7 and C7-T1 (5 horses). Only muscle atrophy was considered to be a clinically relevant ultrasonographic finding in this group. The synovial effusions were considered secondary to joint instability.
Transverse ultrasonographic images of the left (A) and right (B) supraspinatus and infraspinatus muscles at the time of initial examination in a 5-year-old Thoroughbred with a predominant injury to the right suprascapular nerve. Notice the severe atrophy of the right supraspinatus and infraspinatus muscles, compared with the muscles of the contralateral limb, with increased echogenicity of the muscle body indicating fibrosis. LF = Left forelimb. RF = Right forelimb.
Citation: Journal of the American Veterinary Medical Association 249, 10; 10.2460/javma.249.10.1187
Treatments were recorded for 3 horses and included mesotherapy over the affected shoulder and neck region (n = 3 horses), electrostimulation (1), and ultrasound-guided perineural injection of the suprascapular nerve with a nanopolysaccharide solution used as a regenerating agent (1). No horses had surgical treatment.
After the initial examination at the study facility, 2 of 4 nonlame horses in the group were returned to their activities immediately (at decreased intensity for a mean of 2 months). Nine horses were managed conservatively by stall rest with a mean duration of 6.4 months (median, 6 months; range, 2 to 11 months), followed by progressive training for a mean duration of 4 months (median, 4.5 months; range, 3 to 5 months). Six horses had clinical improvement (return of joint stability, muscle mass, or both), noticed ≤ 2 months (n = 1), 3 to 4 months (1), and ≥ 6 months (4) after the onset of clinical signs. Clinical improvement was reported by the referring veterinarian and the owner or trainer for all horses and was observed at the study facility for 2 of these horses. Progressive decrease in synovial effusion and recovery of muscle mass were observed by ultrasonography of these 2 horses at the facility during rehabilitation.
Eight of 11 horses had a positive outcome, having returned to athletic soundness or to their intended or previous use, including flat racing (n = 3), racing as trotters (2), show jumping (1), general riding (1), and breeding (1). Among these 8 horses, 3 were sound despite persistence of mild to marked atrophy of the infraspinatus muscle, 1 (a French Trotter) raced successfully despite persistence of mild (grade 1) lameness, and the remaining 4 were sound with no apparent abnormalities. The mean recovery time for the 8 horses with a positive outcome was 9.3 months (median, 6 months; range, 5 to 16 months). Three horses had negative outcomes. Two were retired because of persistent shoulder joint instability and lameness despite long periods of rest, and 1 was retired to become a broodmare without being returned to the previous activity. This horse had fully recovered from the initial injury after being retired (with no clinical signs of neuropathy and good stability of the shoulder joint).
Axillary nerve injuries
Two horses (a 1-year-old Thoroughbred colt and a 4-year-old warmblood stallion that was used for show jumping) were classified as having axillary nerve injuries. These horses were examined because of muscle atrophy in the shoulder region of 2 weeks' and 1.5 months' duration, respectively. One horse had a known history of trauma, and trauma was suspected in the other. The left shoulder region was affected in both animals.
At the time of the referral examination, both horses had marked atrophy of the deltoideus muscle and 1 had atrophy of the cleidobrachialis muscle (Figure 2). No other gross abnormalities were observed.
Photograph of the left shoulder region of a 1-year-old Thoroughbred with a predominant injury of the left axillary nerve, showing atrophy of the deltoideus (black arrowhead) and cleidobrachialis muscles (white arrow).
Citation: Journal of the American Veterinary Medical Association 249, 10; 10.2460/javma.249.10.1187
Both horses were sound on lameness evaluation at a trot. One horse had a mildly decreased cranial phase of the step of the affected limb, compared with that of the contralateral limb, and had mild instability of the shoulder joint.
Radiographic examination included views of the affected shoulder joint and cervical spine in both horses and the elbow joint in 1 horse. Neither horse had radiographic abnormalities detected. The shoulder area was examined ultrasonographically, and clinically relevant muscle atrophy was identified in both horses. The deltoideus muscle was affected in both horses, and the cleidobrachialis muscle was affected in 1. One horse had synovial effusion of the scapulohumeral joint (deemed secondary to joint instability), and the other had osteoarthrosis of C7-T1; neither finding was considered clinically important.
Both horses were managed conservatively with stall rest (n = 1 horse) or pasture rest (1). The mean recovery time was 3.5 months. Both horses were treated with physiotherapy (including electrostimulation and stretching, with or without massage), and the adult horse received specific flat work exercises (eg, half-pass and shoulder-in movements) introduced gradually after the period of pasture rest. One horse was reexamined at the study facility, and both horses had a positive outcome despite persistence of deltoideus muscle atrophy (severe in one horse and mild in the other). No forelimb lameness was reported during the follow-up period.
Predominant radial nerve injuries
Horses grouped as having radial nerve injuries (with or without other nerve injuries) included 3 mares or fillies, 3 geldings, and 8 stallions or colts. Breeds or breed types included Thoroughbred (n = 1), French Trotter (5), and warmblood (8). Mean age was 3.7 years (median, 1.25 years; range, 3 months to 15 years). Adult horses were used for flat racing (n = 1 horse), show jumping (2), and 3-day eventing (2). Eleven horses were examined because of grade 5 lameness with a dropped elbow sign (duration of lameness was ≤ 7 days for 7 horses, ≤ 1 month for 2 horses, and > 1 month for the remaining 2). Three horses were examined because of a 1-year history of failure to protract a forelimb when jumping (n = 1) or because of intermittent forelimb lameness with stumbling of 2 months' duration (1) or underwent a routine clinical examination after a fall 11 months prior to the visit (1).
Six horses had a history of known trauma in the stall, in the pasture, or during competition. Eight had been found with non–weight-bearing lameness in the field. The right forelimb was affected in 8 horses, and the left was affected in 6. Muscle atrophy over the shoulder and elbow areas had been identified in 3 horses by the referring practitioners ≤ 14 days after the onset of lameness. Three horses initially examined for grade 5 lameness were reported to have a mild improvement in lameness grade within 1 month after the onset of clinical signs. Mean duration of clinical signs prior to referral was 65 days (median, 14 days; range, 1 to 365 days). The 11 horses with grade 5 lameness had received anti-inflammatory drugs (NSAIDs [n = 14] and steroids [1]) prior to the referral examination at the study facility.
Physical examination findings for the 11 horses with a history of non–weight-bearing (grade 5) lameness included atrophy over the affected shoulder region, elbow joint, and brachium or antebrachium (6 horses [all examined between 6 days and 3 months after the onset of lameness], including 1 with marked atrophy of the triceps brachii muscle and 5 with marked atrophy of the supraspinatus, infraspinatus, triceps brachii, biceps brachii and extensor carpi radialis muscles; Figure 3). Other findings included contracture of the flexor tendons of the affected limb (1 horse [a yearling]), severe flexural and angular limb deformities (1 [a foal]), and loss of sensory perception distal to the elbow joint (2 [adult horses]). Presence of sensory perception in the affected limb was recorded for 3 horses, but the data were not available for the remaining 6. Muscle atrophy was not detectable in 2 horses with non–weight-bearing lameness but developed in the shoulder region, elbow joint, brachium, and antebrachium shortly after the referral examination. Physical examination findings for the 3 horses that had no history of lameness or a history of intermittent (grade 2) lameness included mild pectoral muscle atrophy (n = 1), mild atrophy of the cranial muscles of the antebrachium (1), marked atrophy of the muscles of the brachium and antebrachium (1), and a scar extending from the shoulder to the brachium (1).
Photograph (obtained on initial evaluation) of the right shoulder and forelimb of a 3-year-old warmblood with a predominant injury of the right radial nerve. The horse was evaluated because of a 2-month history of non–weight-bearing lameness of the affected limb. Notice the distal displacement of the olecranon tuberosity (ie, dropped elbow sign) and marked atrophy of the muscles of the shoulder, brachium, and antebrachium.
Citation: Journal of the American Veterinary Medical Association 249, 10; 10.2460/javma.249.10.1187
On examination while trotting in a straight line, 11 horses had grade 5 lameness, had a dropped elbow sign, and were unable to extend the distal aspect of the affected limb. One horse had grade 2 lameness with a tendency to stumble. The 2 other horses were found to be sound on lameness examination, but 1 had a lack of protraction of the affected limb when jumping, and 1 had a mild instability of the affected shoulder and elbow joints when walking or trotting.
Radiographic examination of these horses included views of the affected shoulder joint (n = 13 horses), elbow joint (14), cervical spine (4), and humerus (3). Findings included mild scapulohumeral dysplasia with discrete periarticular bone remodeling, fracture of the epicondylar crest of the humerus, and medial opening of the elbow joint space (1 horse each). The radiographic abnormalities were not considered clinically important as related to the lameness; in the horse with fracture of the epicondylar crest, clinical signs were attributed to injury of the radial nerve at the dorsal aspect of the elbow. Ultrasonographic examination included the affected shoulder area (n = 14), elbow region (12), and brachium (1) as well as the neck (3). Two horses had no abnormality detected, 1 had 1 abnormality detected, and the remaining 11 had ≥ 2 abnormalities detected. Findings included clinically relevant marked atrophy of the supraspinatus (n = 2 horses), infraspinatus (3), triceps brachii (6), biceps brachii (5), and extensor carpi radialis muscles (3). Arthrosis of the C6-C7 and C7-T1 articular process joints, potentially responsible for compression of the nerve roots, was found in 2 horses. Other findings included synovial effusion of the elbow joint (n = 6), bicipital bursa (4), or scapulohumeral joint (3), which were attributed to joint instability and not considered clinically important, and hematoma in the supraspinatus muscle (1), which was considered secondary to the trauma.
Treatments recorded for horses with grade 5 lameness included systemic administration of NSAIDs (n = 1 horse) or steroids (1), physiotherapy (stretching, massage, or both; 5), ultrasound-guided injection of a nanopolysaccharide (regenerating agent) solution into a muscular hematoma (1), and oral administration of homeopathic agents (1). Three of these horses received > 1 type of treatment, and 5 horses received no treatment other than stall rest. Treatment of the 3 horses that were sound or had grade 2 lameness included ultrasound-guided intra-articular injections of corticosteroids into the C6-C7 and C7-T1 articular process joints (n = 2), specific flat work exercise (eg, half-pass and shoulder-in movements; 2), and electrostimulation (1).
After the consultation, 3 horses (sound or with grade 2 lameness) were returned to their normal activities. The 11 horses with grade 5 lameness were managed conservatively. This began with stall rest for a mean duration of 6 months (median, 4 months; range, 0.5 to 12 months) and was followed by pasture turnout for a mean duration of 7.7 months (median, 7.3 months; range, 2 to 12 months). Training was then resumed progressively for all adult horses. The mean recovery time was 13.3 months (median, 8 months; range, 0.5 to 24 months).
Follow-up information was available for all 14 horses, including 4 that were reexamined at the study facility. The 3 horses that were sound or had grade 2 lameness on initial evaluation at the study facility each had a positive outcome. When returned to their intended use, these 3 horses still had clinical signs of paresis of the affected limb, including instability of the shoulder (n = 2, including 1 horse reexamined at the study facility) and elbow (1), stumbling (2), and lack of protraction of the affected limb over jumps (1). Locomotion reportedly improved during training for these 3 horses.
Six of 11 horses with grade 5 lameness had a positive outcome (1 of these was later euthanized for an unrelated medical reason). Two of these horses recovered in 2 weeks without developing any muscle atrophy (including the horse later euthanized for an unrelated cause). For 3 other horses that had muscle atrophy evident on initial examination at the study facility (n = 1) or that developed the condition shortly afterward (2), muscle atrophy was no longer detectable at a mean of 17 months after the onset of lameness (median, 14 months; range, 4 to 36 months). These 3 horses were sound with no apparent gait abnormalities at the end of the recovery period. The 1 remaining horse still had signs of muscular atrophy and paresis of the affected limb (including instability of the shoulder, stumbling, and lack of protraction of the affected limb over jump) at the end of the recovery period but was reported to have fully recovered after 1 year of training. The remaining 5 of 11 horses with grade 5 lameness had negative outcomes and were euthanized a mean of 3 months (median, 5 months; range, 1.5 to 6 months) after the onset of clinical signs owing to lack of clinical improvement (including progressive development of contracture of the flexor tendons with severe flexural and angular deformity of the contralateral forelimb [in 2 foals]). Financial reasons, clients unwilling to pursue treatment or provide long-term care, or a combination of these factors were other reasons that led to euthanasia.
Discussion
In the present study, we identified 27 horses with peripheral neuropathy of a forelimb that were evaluated at 2 veterinary referral centers over a 13-year period. This suggested that this condition is uncommon or underdiagnosed or that such horses are infrequently seen at referral centers. Horses that have a rapid improvement in clinical signs would typically not be referred for further evaluation, whereas other horses might have conservative management without further investigation or be euthanized because of a belief of poor prognosis or a suspicion of other severe conditions such as limb fracture.
Trauma (including pressure, stretching, and transection)6,11 is the most frequent cause of peripheral neuropathy of a forelimb in horses. In this study, trauma was the known (10/27 [37%]) or suspected (13/27 [48%]) cause of the condition in most horses. Thirteen horses were found lame in the field or in their stalls. Five horses were seen to collide with a tree or with another horse during training or competition, and 5 were known to have fallen while turned out in a paddock or during competition.
Neurogenic muscle atrophy is a consistent physical sign of peripheral neuropathies, and its severity depends on the nature and duration of the lesion.6,9,14,16,17 In this case series, muscle atrophy was evident in 22 of 27 (81%) horses at the time of examination on referral to the study facility. Atrophy of muscles corresponded to the affected nerves: atrophy of the supraspinatus muscle, infraspinatus muscle, or both was found in all horses with a predominant injury of a suprascapular nerve, and atrophy of the deltoideus muscle was found in 2 of 2 horses with a lesion of an axillary nerve. Atrophy of these muscles and other muscles of the shoulder region, brachium, and antebrachium was found in horses with a radial nerve lesion alone or in association with other nerves.
One important limitation of the present study was that electromyography was not performed in any of the horses. By evaluating and recording the muscular electrical activity more than 7 days after the onset of clinical signs,6–8,14,16,17,23 it is possible to precisely localize denervated muscles and determine affected nerves.8,10,16 With the diagnostic modalities used in the present study, it was not possible to rule out injury of the brachial plexus or of ventral roots of the cervical nerves on the affected side when involvement of > 1 nerve was suspected.11,19 Other limitations of the study included the small number of horses in each group (especially those with axillary nerve injuries), which prevented statistical comparisons, and its reliance on owner and veterinarian memory regarding the evolution of cases for 15 horses examined > 5 years previously (ranging to 14 years) and the subjective input of owners and veterinarians with regard to recovery and patient outcome.
In this study, 11 of 11 horses with a predominant injury to a suprascapular nerve had instability of the affected shoulder joint with abnormal lateral deviation at a walk. This results from a functional deficiency of the muscles of the lateral aspect of the shoulder (supraspinatus and infraspinatus muscles),6,7,9,10,12–17 which have a critical part in the cranial and lateral stabilization of the shoulder joint,19 especially during the stance phase of a stride. Although instability of the shoulder joint has been reported after blocking of the suprascapular nerve at the scapula neck,13 it has also been suggested that other nerves (including the axillary and subscapular nerves as well as roots of the brachial plexus19) are usually damaged with this type of injury, contributing to the clinical signs.11,20 Injuries of the suprascapular nerve leading to neurogenic atrophy of the supraspinatus and infraspinatus muscles have also been described without associated instability of the shoulder joint.19 This corresponds to the finding that 3 horses with suprascapular nerve injury in the present study were sound at the time of follow-up with no sign of instability of the affected shoulder, despite persistence of a mild to marked atrophy of the infraspinatus muscle. Our interpretation was that the surrounding muscles (eg, the deltoideus muscle in these horses with atrophy of the supraspinatus or infraspinatus muscles [or both]) may have compensated for the deficit or that fibrosis of the affected muscles may have provided lateral support. However, it is possible to have instability of the shoulder joint without atrophy of supraspinatus and infraspinatus muscles in the event of a recent nerve injury, if the principle injury involves nerves innervating muscles on the medial aspect of the shoulder, or in patients with mild neurologic injury (neurapraxia or axonotmesis) resulting in paresis.
Most (7/11) horses with predominant suprascapular nerve injury had a mild to marked lameness, and 5 had a reduced cranial phase of the step of the affected limb, compared with that of the contralateral limb. This lack of protraction is another common but less consistent sign associated with injuries to the shoulder region and is not specific to injuries of the suprascapular nerve, because numerous muscles are involved in the cranial phase of the step.28
In accordance with results of a previous study,23 neither of the 2 horses with a predominant axillary nerve injury in the present study was lame. One of these 2 horses had mild reduced protraction of the affected limb and a mild instability of the shoulder joint, confirming involvement of the deltoideus muscle in shoulder joint stability, but to a lesser extent than the supraspinatus and infraspinatus muscles.28
Eleven of 14 horses with predominant radial nerve injury had typical signs of radial nerve paralysis, with a dropped elbow appearance, inability to flex the shoulder joint or extend the distal part of the affected limb, and severe to non–weight-bearing lameness with toe-dragging.6,10,19–21 Milder clinical signs were observed in the other 3 horses of this category, including muscle atrophy (pectoral muscle or cranial muscles of the brachium and antebrachium), grade 2 lameness with a tendency to stumble, slightly reduced protraction of the affected limb when jumping, and mild instability of the affected shoulder and elbow joints; these clinical findings might have reflected less severe nerve damage in these horses. Clinical improvement had been observed in 7 of 27 (26%) horses between the onset of injury and evaluation at a study referral center. This most likely corresponded to lessening of pain and inflammation associated with the initial injury and, in some horses, to progressive reinnervation of the affected muscles.10,14
For the horses in this case series, the diagnosis of peripheral neuropathy was made after exclusion of other potential causes of lameness, such as fractures or arthropathies, which is consistent with other published reports.14,17,20,21 Radiographic examination failed to reveal osteoarticular abnormalities that, taken alone, could result in the observed clinical signs in any horse. In 2 horses, osteoarthrosis of the articular process joints of C6-7 and C7-T1 was considered to potentially cause impingement on or compression of the nerve roots.29 However, as this condition does not induce specific muscle atrophy, it was not considered responsible alone for the clinical signs. These horses underwent ultrasound-guided injection of corticosteroids into the affected cervical joints as part of their treatment.
Ultrasonography has been reported to provide accurate information on muscle atrophy (in terms of localization, nature [disuse vs denervation], severity, and changes over time)30 and on synovial effusion accompanying joint instability,31 making it an indispensable diagnostic tool. No specific sophisticated equipment is required to scan forelimbs or the caudal region of the cervical spine in horses. In the present study, 25 of 27 (93%) horses had abnormal ultrasonographic findings attributed to the initial trauma or considered secondary to the neuropathy and subsequent joint instability. Muscle atrophy was detected by this method in 22 of 27 (81%) horses. Ultrasonography can be used to differentiate between atrophy secondary to denervation and that resulting from disuse; in disuse, the overall volume of the muscle is decreased, but its echogenicity is normal (hypoechogenic with a speckled appearance except for interspersed bright lines from perimysium). When atrophy is the result of a denervation process, the muscle body appears more echogenic than usual (similar to the echogenicity of tendons) with a more homogeneous architecture (reduced muscle fiber content with denser interfascicular connective tissue). However, in patients with neurogenic atrophy, ultrasonography does not allow for differentiation among injuries of peripheral nerves, nerves of the brachial plexus, and spinal nerve roots.
Synovial effusion of the scapulohumeral joint, elbow joint, or bicipital bursa was visualized by ultrasonography in 19 of 27 (70%) horses of the present study, and the degree of synovial effusion corresponded to the severity and the duration of joint instability. During the follow-up period, repeated ultrasonographic examinations were performed in 7 of 27 horses. Together with a regular clinical follow-up, ultrasonography can provide information on the reinnervation process and on response of the affected joint to instability (eg, changes in the degree of synovial effusion over time or development of degenerative arthritis).
Mean recovery time (duration from the onset of the clinical signs to the time the horse was returned to its previous or intended use) was 9.3 months, 3.5 months, and 13.3 months for horses with predominant suprascapular nerve, axillary nerve, and radial nerve injuries, respectively. It has been suggested that suprascapular nerve function should return within approximately 70 days after injury in horses.16 This was estimated on the basis of the distance between the typical site of injury at the cranial border of the scapula and the infraspinatus muscle (approx 6.5 cm) and the rate of nerve regeneration (approx 1 mm/d).16 For more proximal sites of injury (including the brachial plexus or the ventral nerve roots of the contributing nerves), the regeneration process would be expected to require more time. Results of this case series suggested that reinnervation and resolution of specific gait abnormalities may require up to 24 months in some horses.
In the present study, 5 horses with predominant radial nerve injury were euthanized ≤ 6 months after the onset of severe (grade 5) lameness. These horses were euthanized because of the client unwilling to pursue treatment or provide long-term care, absence of clinical improvement, financial concerns, or a combination of these; it is possible that additional time would have been beneficial to some of these horses.
Follow-up information for the horses of this report suggested that the prognosis for return to athletic activity after peripheral nerve damage affecting a forelimb is favorable overall, considering that 19 of 27 (70%) horses (including 1 subsequently euthanized for an for unrelated reason) had a positive outcome, regardless of the treatment, which was primarily conservative. This was not a prospective, placebo-controlled study, and therefore assessment of efficacy of the various treatments was not possible. It should also be noted that not all of the treatments administered to horses in this study are commercially available and legal for use in the United States. Persistence of a mild to moderate degree of muscle atrophy is common and does not appear to prevent horses from being competitive once the other clinical signs have subsided.10,14 According to the literature, long-term prognosis for horses with lesions of a suprascapular or axillary nerve is good.14,16 Results of the present study, in which 10 of 13 horses with suprascapular or axillary nerve injury alone had a positive outcome, were consistent with that information. Prognosis following injury to a radial nerve is reportedly good if clinical improvement is noticed within 2 to 4 weeks after the onset of clinical signs10,20 and guarded if clinical signs persist for > 6 months.10,21 In the present study, 9 of 14 horses with predominant radial nerve injury had a positive outcome, including 6 of 11 horses that initially had severe (grade 5) lameness. Some of these horses required up to 12 months of stall rest before signs of improvement (sufficient to allow pasture rest or a gradual reintroduction to exercise and training) were observed; in some horses with radial nerve paralysis, muscle atrophy worsened during the first few weeks of stall rest.
Results for horses with peripheral neuropathy of a forelimb in this study suggested that conservative management including an extended period of rest followed by controlled exercise can lead to a positive outcome, with many horses returning to their previous level of athletic activity. For these horses, the long-term outcome (≥ 9 months after the initial consultation) was favorable overall, but case management should be modified depending on the clinical evolution of the patient and the development of tendinous contracture. Our results suggested that the severity of the initial clinical signs may not be a good indicator of the final outcome for horses with these conditions, and that a prolonged recovery time (> 12 months) may be required for most horses with such injuries. Further prospective research including larger numbers of horses is needed to confirm these findings and to determine optimal treatment strategies.
Acknowledgments
Supported by the Conseil Régional de Basse-Normandie and the European Parliament (European Regional Development Funds).
The authors declare that there were no conflicts of interest.
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