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IN-DEPTH: NEUROLOGY

Diseases of the Peripheral , Neuromuscular Junction, or Uncertain Sites: Relevant Examination Techniques and Illustrative Video Segments

Robert J. MacKay, BVSc (Dist), PhD, Diplomate ACVIM

Author’s address: Alec P. and Louise H. Courtelis Equine Teaching Hospital, College of Veterinary Medicine, University of Florida, Gainesville, FL 32610; e-mail: mackayr@ufl.edu. © 2011 AAEP.

1. Introduction troversial issue. Peripheral are Mechanical injuries to peripheral nerves occur be- characterized by weakness of the innervated muscle cause of compression, entrapment, transection, lac- accompanied within 2 to 4 weeks by appreciable eration, ischemia, crushing, stretching, or chemical atrophy. When the injured nerve supplies impor- or burn damage.1,2 Neurapractic lesions are charac- tant extensor muscles of the limbs (e.g., as is the terized by a failure of conduction of the action po- case for radial, femoral, sciatic, and peroneal tential across the injured axonal segment.3 nerves), there is obvious alteration of gait. Areas of is axonal interruption caused by axon cutaneous occasionally accompany pe- and myelin sheath , whereas neurotmesis re- ripheral nerve injuries. Over the neck and trunk, flects complete disruption of endoneurium, perineu- cutaneous sensory innervation occurs in defined rium, and/or epineurium. Recovery by axonal bands associated with segmental dermatomes. regrowth is unlikely after neurotmesis.4 After ax- Damage to a peripheral spinal nerve or dorsal nerve onotmesis of motor nerves, muscle reinnervation is root results in cutaneous anesthesia/hypalgesia over to be expected and occurs by 2 separate mecha- the supplied dermatome. With damage to the pu- nisms: collateral sprouting and axonal regrowth.1 dendal nerve or its sacral nerve roots, there is anes- If there is incomplete loss of axons, reinnervation of thesia/hypalgesia of the perineal area. In contrast, muscle units by sprouting occurs in days to weeks. relatively small autonomous zones have been de- Reinnervation by axonal regrowth occurs at a rate of fined for sensory components of the ulnar, musculo- 1 millimeter per day (approximately 1 inch per cutaneous, median, femoral, tibial, and peroneal month). Skeletal muscle cells deprived of nerve nerves.5,6 Sympathetic fibers are distributed with supply ultimately undergo fibroblastic transforma- peripheral nerves, so denervated skin also may be tion; thus, reinnervation may not be possible after evident as circumscribed spontaneous sweating. more than 12 months, although this remains a con- The most common and important syndromes of me-

NOTES

AAEP PROCEEDINGS ր Vol. 57 ր 2011 363 IN-DEPTH: NEUROLOGY chanical injury to peripheral nerves of the limbs are mon and causes only transient toe-dragging. The described below.6–8 shoulder may be held in a flexed position and the elbow in an extended position. There is hypalgesia/ 2. Suprascapular Nerve anesthesia over the dorsomedial aspect of the knee The suprascapular nerve arises from C6 and C7 and proximal metacarpus and atrophy of the biceps segments. Injury occurs most com- and brachialis muscles. monly when a horse’s shoulder is impacted at speed such that the nerve is injured as it curls around the 5. Median and Ulnar Nerves front of the neck of the scapula. There immediately The median nerve arises from C8 and T1 and the is laxity and lateral instability of the shoulder joint, ulnar nerve from T1 and T2. Injury to either can be which bows out or “pops” as the affected limb bears caused by injury to the brachial plexus or along the weight. Within 2 to 4 weeks of injury, there is medial aspect of the upper limb. Clinical findings obvious atrophy of the supraspinatus and infraspi- include a “tin soldier” gait, with decreased flexion natus muscles (Sweeney). At least 50% of such in- and dragging of the toe during protraction of the juries are predominantly neurapractic, and recovery limb and hypalgesia/analgesia of the skin of the of function (and muscle mass as there is atrophy) is caudal forearm, lateral metacarpus, and medial pas- evident within 30 days of injury and is complete tern areas and atrophy of the carpal and digital within 60 days. In more severe injuries with mor- flexors. bid axonal injury, successful reinnervation is evi- dent as recovery of muscle bulk in the ventral part of 6. Femoral Nerve the supraspinatus muscle beginning within 3 The femoral nerve arises from L3 to L5 and inner- months of injury. Maximal recovery takes an addi- vates muscles that flex the hip and extend the stifle. tional 3 to 12 months. Regrowth of the suprascap- The nerve can be damaged by ilial, femoral, or ver- ular nerve can be facilitated by surgery to resect tebral fractures. Ischemic injury is caused by pro- scar tissue and a constricting band (external neurol- longed stretch or increased tissue pressure during ysis) and reduce tension on the nerve as it crosses anesthesia in dorsal recumbency or after severe pro- the front of the scapula (often performed 3 to 6 longed dystocia.11 With unilateral paralysis, the months after injury). Removal of a piece of bone pelvic limb is abnormally flexed, usually with the from the neck of the scapula may further relax the foot flat on the ground, and buckles when the limb injured nerve, but the scapular notch created by this bears weight. In the case of bilateral involvement, procedure creates a potential nidus for scapular the horse is either unable to rise or stands uncom- fractures during recovery from anesthesia. fortably in a crouched position. If the occurs proximal to the saphenous branch, there is 3. Radial Nerve anesthesia/hypalgesia of the skin over the medial The radial nerve innervates a flexor of the shoulder surface of the thigh and atrophy of the quadriceps and the extensors of the elbow, carpal, and digital muscle. joints. It arises from T1. The may be lacerated by fractures of the C7 or T1 vertebrae or 7. Sciatic Nerve first rib. The nerve is commonly damaged as a The sciatic nerve arises from L5-S1 and supplies result of humeral fracture9 and can be injured important extensors of the hip and flexors of the within the brachial plexus by trauma to the shoul- stifle. Damage usually is a result of deep injections der region. Ischemic damage may occur in horses into the caudal thigh.1 The nerve also may be in- anesthetized in lateral recumbency.10 The lower jured by fractures of the ilium or ischium or sacro- part of the nerve may be injured by dislocation or iliac or coxofemoral dislocations. The limb is held fractures that involve the elbow. slightly caudal with the dorsum of the hoof resting Horses with complete radial paralysis stand with on the ground. The stifle and hock are extended, the shoulder extended, the elbow “dropped,” and the whereas the distal joints are flexed. The leg is dorsum of the hoof resting on the ground. When dragged forward by the actions of the quadriceps forced to walk, the horse may partially protract the and biceps femoris muscles. These muscles, in con- limb by exaggerated extension of the shoulder; how- cert with the reciprocal apparatus, allow the horse ever, the toe drags and the horse collapses on the to bear some weight on the limb if the foot is first limb during the weight-bearing phase of the stride. placed in normal position. There is cutaneous hyp- If the site of damage is distal, the shoulder and algesia/anesthesia over most of the limb except for elbow are normal. Although the radial nerve has the medial thigh. numerous cutaneous sensory branches, injury to this nerve does not result in any consistent area of 8. Peroneal Nerve cutaneous anesthesia. The peroneal nerve arises from the sciatic trunk deep to the biceps femoris and is motor to the flexors 4. Musculocutaneous Nerve of the tarsus and the extensors of the digit. Paral- The musculocutaneous nerve arises from C7 and C8 ysis results in extension of the tarsus and flexion of and supplies flexors of the elbow. Injury is uncom- the distal joints of the pelvic limb. At rest, the limb

364 2011 ր Vol. 57 ր AAEP PROCEEDINGS IN-DEPTH: NEUROLOGY is held slightly caudally with the distal joints in sensation at each site by grasping a fold of skin flexed position and the dorsum of the hoof contacting between the jaws of the hemostat then firmly the ground. During walking, the limb is moved squeezing the skin and watching for evidence of a erratically. The toe is dragged along the ground conscious response by the horse. This is a behav- during the weak protraction phase, then is pulled ioral reaction and must be distinguished from a caudally as the horse attempts to bear weight. reflex that may occur without cognitive acknowl- There is atrophy of the cranial tibial and long and edgement. Sensory fields for some peripheral lateral digital extensors and immediate cutaneous nerves of horses have been described.6 hypalgesia/anesthesia over the lateral metatarsus. Test pelvic limb reflexes and function: First, as- sess extensor tone in the limb by testing resistance 9. Tibial Nerve to passive flexion. Next, perform the flexion test by The tibial nerve is the direct continuation of the pinching skin on the distal limb with a hemostat. sciatic nerve and innervates the gastrocnemius (ex- If there is no response, try pinching skin elsewhere tensor of the hock) and digital flexors. The limb is on the leg. A normal response is flexion of the limb, held flexed and the foot contacts the ground in nor- usually with some behavioral evidence that the mal position, the fetlock often partially collapses horse can feel the skin pinch. When abnormal, the into a flexed position (i.e., “knuckles”). The foot is flexor response may be reduced or absent and may moved in stringhalt-like fashion, with exaggerated be accompanied by reflex extension of the contralat- flexion of the hock and stifle during protraction fol- eral digit (crossed extensor reflex). To test the pa- lowed by sudden extension to the weight-bearing tellar reflex, hold the pelvic limb in a moderately phase of the stride. There is atrophy of the gastroc- flexed position, and strike the skin over the middle nemius and cutaneous hypalgesia/anesthesia of the patellar ligament. A twitch handle works well for caudal metatarsal region and bulbs of the heels. this purpose in full-sized horses; a patellar hammer The flexor reflex is tested by pinching the skin over or reversed hemostat can be used in foals. The the dorsal aspect of the fetlock. The reflex is pres- expected response is brisk extension of the stifle. ent but weaker than on the normal side. If the reflex is absent, move the leg into different positions and retest. Classify the response as ab- 10. Prognosis for Peripheral Nerve Injury sent, normal, or increased. Other extension re- With suprascapular neuropathy secondary to con- flexes in the pelvic limb cannot be elicited reliably firmed or suspected shoulder trauma, restoration of but should be tested for comparison with the oppo- shoulder stability occurred in 3 to 12 months in 7 of site leg. These include (1) the tibial reflex: tap the 8 horses treated only with stall rest.12 Atrophy of biceps femoris just behind the greater trochanter; the infraspinatus and supraspinatus resolved in (2) the gastrocnemius reflex: strike the Achilles ten- only 2 of these horses. Although there is no com- don close to its insertion; and (3) the cranial tibial parative study to show any additional effect of pro- reflex: strike the middle of the cranial tibial muscle. cedures to relieve entrapment of the suprascapular Test thoracic limb reflexes and function: Assess nerve,13,14 it is expected that these procedures extensor tone and evaluate the flexor reflex as de- should improve recovery of muscle mass. Data for scribed for the pelvic limb. No other reflex can be outcome of radial nerve neuropathy are not pub- obtained consistently in the thoracic limbs but, for lished; however, it is reasonable to assume that the comparison with the opposite limb, test the follow- prognosis for complete recovery from signs of radial ing: (1) triceps reflex: with the limb in flexed posi- paralysis induced by positioning in lateral recum- tion, strike the triceps muscle and watch for elbow bency, soft-tissue trauma, and humeral fracture is extension; (2) biceps reflex: strike the front of the good (Ͼ80%), fair, and poor, respectively. Injec- elbow and watch for extension of the shoulder and tion-associated neuropathy (usually sciatic) typi- flexion of the elbow joint; and (3) strike the middle of cally resolves in days. the extensor carpi radialis muscle and look for ex- tension of the carpus. 11. Neurologic Testing of Recumbent Horses Lesion Location Examination If a horse can dog-sit, the principal spinal cord lesion The examiner should carefully note whether or not probably is behind T2. Inability of a horse to roll the horse moves its limbs voluntarily without stim- from lateral into sternal recumbency is associated ulation. If possible, assist and stimulate the horse with severe lesions (usually involving gray matter) in such a way as to assess which of the following best of the caudal cervical and/or cranial thoracic seg- describes the horse’s maximal voluntary motor func- ments, whereas serious injury to the spinal cord in tion: (1) lifts head off the ground; (2) rolls shoulders the rostral part of the neck may also prevent a horse and chest into a sternal position, or; (3) straightens from raising its head off the ground. thoracic limbs and assumes a “dog-sitting” position. With involvement of lower motor neurons to limb The long spinal reflexes (cervicofacial, cutaneous muscles, there is reduced or absent extensor tone. trunci, slap) and cutaneous sensation over the limbs Limb reflexes are reduced or abolished if the sensory and torso should be evaluated systematically. Test nerves, motor nerves, or central components of the

AAEP PROCEEDINGS ր Vol. 57 ր 2011 365 IN-DEPTH: NEUROLOGY reflexes are affected. In contrast, extensor tone they pass through the sacrum and proximal coccy- and limb reflexes may be exaggerated beginning geal vertebrae. several days after injury to descending upper motor neurons. For example, after trauma to the spinal Associated Clinical Signs cord at the T13 segment, patellar reflexes and pelvic With involvement of S2 and more cranial nerve extensor muscle tone may be exaggerated. roots, expect to see signs of pelvic limb weakness in If there is no response to strong pinching of the addition to cauda equina syndrome. Colic caused skin over caudal regions of the body, there probably by obstipation may be the presenting sign of rectal is catastrophic damage to the spinal cord cranial to paralysis, and urinary overflow incontinence is a the anesthetic area. If there is no response to deep sign of bladder paralysis. pain for more than 24 hours, there is at least func- References tional transection of the spinal cord. 1. Hermann RC Jr. Mechanical injuries. In: Noseworthy JH. Neurological therapeutics: Principles and practice. London: Associated Clinical Signs Martin Dunitz, 2003;1953–1968. Large horses that remain recumbent for more than a 2. Spinner RJ, Kline DG. Surgery for peripheral nerve and few hours often have reduced skin sensation in the brachial plexus injuries or other nerve lesions. Muscle Nerve 2000;23:680–695. distal limbs secondary to pressure-induced injury of 3. Grant GA, Goodkin R, Kliot M. Evaluation and surgical superficial sensory nerves. This complicates inter- management of peripheral nerve problems. pretation of tests for flexor reflexes and for presence 1999;44:825–839. of deep pain. 4. Smith ML, Bauman JA, Grady MS. Neurosurgery. In: Brunicardi FC, Andersen DK, Billiar TR, et al. Schwartz’s principles of surgery. 9th ed. Columbus: McGraw-Hill, 2005. 12. Tail and Anus 5. Blythe LL, et al. Am J Vet Res 1982;43:1511. 6. Mayhew IG. Large animal neurology. 2nd ed. Oxford: Wiley- Examination Blackwell, 2008. Assess tail strength by lifting (extending) the tail. 7. Hahn CN, Mayhew IG, MacKay RJ. Examination of the ner- Prod or pinch the skin adjacent to the anus and vous system. In: Colahan PT, Mayhew IG, Merritt AM, Moore JN. Equine medicine and surgery. 5th ed. St. Louis: observe the anal contraction and tail-clamp reflexes. Mosby, 1999;972–996. If these reflexes are abnormal or if the history sug- 8. George LW. Diseases of the nervous system. In: Smith BP. gests possible cauda equina syndrome, perform a Large animal internal medicine. 4th ed. 2008. rectal examination to assess rectal tone and bladder 9. Rooney JR. Radial paralysis in the horse. Cornell Vet size and tone. Assess muscular symmetry of the 1963;53:328–338. 10. Schmelzer JD, Zochodne DW, Low PA. Ischemic and reper- tail and test cutaneous sensation over the tail and fusion injury of rat peripheral nerve. Proc Natl Acad Sci caudal structures. USA1989;86:1639–1642. 11. Dyson S, Taylor P, Whitwell K. Femoral nerve paralysis Lesion Location after general anesthesia. Equine Vet J 1988;20:376–380. 12. Dutton DM, Honnas CM, Watkins JP. Nonsurgical treat- Anesthesia and areflexia of the tail, penis, and ment of suprascapular nerve injury in horses: 8 cases perineum and paralysis of the anus, rectum, blad- (1988–1998). J Am Vet Med Assoc 1999;214:1657–1659. der, and penis are signs of cauda equina syndrome. 13. Adams OR, Schneider RK, Bramlage LR, et al. A surgical Lesions of the spinal cord or nerve roots caudal to approach to treatment of suprascapular nerve injury in the horse. J Am Vet Med Assoc 1985;187:1016–1018. the S2 spinal cord segment cause some to all of the 14. Schneider JE, Adams OR, Easley KJ, et al. A surgical ap- signs of cauda equina syndrome. The bundle of proach to treatment of suprascapular nerve injury in the roots forming the cauda equina are vulnerable as horse. J Am Vet Med Assoc 1985;187:1019–1020.

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