256 Vol. 25, No. 4 April 2003
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1 256 Vol. 25, No. 4 April 2003 CE Article #1 (1.5 contact hours) Refereed Peer Review Comments? Questions? compendium@medimedia.com Web: VetLearn.com Fax: KEY FACTS Primary injury refers to spinal cord, meningeal, and vascular damage directly related to the disk herniation. The following four interrelated pathophysiologic mechanisms contribute to secondary injury: Spinal cord ischemia Production of free radicals (reperfusion injury) Electrolyte abnormalities Neutrophil and macrophage activation Ascending descending diffuse myelomalacia is an infrequently seen trauma and may lead to death by respiratory paralysis. Loss of Deep Pain Sensation Following Thoracolumbar Intervertebral Disk Herniation in Dogs: Pathophysiology Purdue University West Lafayette, Indiana Pierre M. Amsellem, DEDV* James P. Toombs, DVM, MS, DACVS Pete H. Laverty, BVSc, MACVSc, DACVS Gert J. Breur, DVM, PhD, DACVS ABSTRACT: Spinal cord injury following intervertebral disk herniation is a combination of a concussive and a compressive injury. Concussion of the spinal cord acutely damages meninges, blood supply, and neural tissue. This constitutes the primary injury. Following the primary injury, a cascade of vascular, biochemical, and cellular events results in additional secondary injury to the spinal cord. Compression of the spinal cord following intervertebral disk herniation may result from a mass of herniated disk material and hematoma within the vertebral canal (extradural compression) or spinal cord swelling within a rigid dura mater (intramedullary compression). Knowledge and understanding of the pathophysiology are important for appropriate diagnosis and treatment of spinal cord injury. The most common cause of spinal cord injury in dogs is intervertebral disk herniation. 1 However, disk herniation does not always result in spinal cord injury. Many herniations remain asymptomatic or cause pain without neurologic dysfunction. Loss of deep pain sensation following thoracolumbar intervertebral disk herniation is the most severe clinical presentation of the related spinal cord injury. It has been thought that the prognosis for these animals was poor; however, recent reports suggest that the prognosis for these injuries may be much better than previously reported. 2 5 This article discusses the pathophysiology of spinal cord injury following intervertebral disk herniation with a special emphasis on spinal cord injury in sensory-negative dogs. *Dr. Amsellem is currently affiliated with the Animal Emergency Clinic, West Palm Beach, Florida.
2 258 Small Animal/Exotics Compendium April 2003 Figure 1A Hansen type I herniation Figure 1B Hansen type II herniation Figure 1 (A) Acute Hansen type I disk herniation, resulting in both concussive and compressive injury (disk material and hematoma remaining in the vertebral canal) to the spinal cord. (B) Slow, progressive Hansen type II herniation, which mainly results in compression of the spinal cord. Blue = annulus fibrosis; green = compressed spinal cord; red = nucleus pulposus. CATEGORIES OF SPINAL CORD TRAUMA Spinal cord trauma associated with intervertebral disk herniation can be categorized as either an acute impact injury (concussion) or as a slow progressive compressive injury of the spinal cord. 6 Concussive injury is usually associated with extrusion of the nucleus pulposus (Hansen type I disk herniation), whereas compression may be associated with either Hansen type I or type II disk herniation (Figure 1). With Hansen type I intervertebral disk herniation, concussion and compression of the spinal cord usually occur concomitantly. The extruded nuclear material and hematoma remain within the vertebral canal and may result in a compressive mass. 7 Concussive Spinal Cord Trauma Primary Injury The primary injury is composed of injury to the meninges, spinal cord, and associated vasculature directly related to the disk herniation. The severity of the primary concussive lesion depends on the mass and the velocity of the disk material extruded into the vertebral canal. 6 Even a small volume of extruded nuclear material can cause severe damage to the spinal cord if it impacts the cord with high velocity. 8 Gray matter is more rigid and fragile than white matter and, therefore, is more susceptible to the disruptive force of a concussive injury. 9 Herniation of an intervertebral disk may also disrupt the spinal cord vasculature (ventral spinal artery and vertical arteries), resulting in ischemic injury to the cord. 10 Under normal conditions, spinal cord blood flow is maintained within narrow limits despite variations in systemic blood pressure (spinal cord blood flow autoregulation). This homeostatic mechanism often fails following spinal cord injury. Primary injury may result in posttraumatic systemic hypotension 11 and reduced spinal cord blood flow, further contributing to ischemia. 12 Secondary Injury Following primary injury, a cascade of vascular, biochemical, and cellular events is initiated, leading to secondary injury. Four interrelated pathophysiologic mechanisms contribute to secondary injury (Figure 2): Spinal cord ischemia Production of free radicals Electrolyte abnormalities Neutrophil and macrophage activation Spinal cord ischemia may initially result from primary injury. Ischemia may progress during the secondary injury. 13 Progressive ischemia of the spinal cord occurs Primary injury Neural, vascular, and meningeal damage Decrease in spinal cord blood flow Secondary injury Ischemia Free radical production Electrolyte abnormalities Neutrophil and macrophage activation Gray and white matter damage Neurologic deficits Diffuse myelomalacia Figure 2 Pathophysiology of spinal cord concussion. This process usually is well established within 8 hours of the injury. In some animals, following a severe concussive injury, the cascade of events continues, producing progressive cord damage over a few days. The damage may extend longitudinally in a cranial and caudal direction from the initial lesion. This is called ascending descending diffuse myelomalacia.
3 260 Small Animal/Exotics Compendium April 2003 following the release of potent vasoactive mediators and free radicals. Prostaglandins and leukotrienes promote platelet aggregation within the spinal cord vasculature. 14 In response to the rapid reoxygenation of the ischemic spinal cord, highly reactive oxygen free radicals, such as superoxide anion, hydrogen peroxide, and hydroxyl radicals, are generated. 15 These molecules are capable of causing cell membrane lipid peroxidation with disruption of neuronal, glial, and endothelial cells. Endothelial cell damage of the spinal cord microvasculature may further exacerbate the ischemic process, yielding lipid peroxides and lipid free radicals, such as malonyldialdehyde and 25-hydroxycholesterol. 16 These substances in turn may disrupt more cell membranes, propagating the pathologic process from cell to cell. 16 It has been suggested that following hemorrhage in the spinal cord, extravasated blood components, such as iron, copper, and hemoglobin degradation products, may catalyze the lipid peroxidation of cellular membranes. 8 Damage to the glial and neuronal membranes results in further neurologic dysfunction. This is called reperfusion injury. Under normal conditions, homeostatic mechanisms maintain intracellular neuronal calcium and sodium concentrations within narrow limits. Following spinal cord injury, neuronal membranes may be disrupted by lipid peroxidation, which permits an influx of calcium and sodium ions into the neuronal cytoplasm with an efflux of potassium. 14 The increased intracellular calcium concentration activates phospholipases that further disrupt cell membranes with the release of arachidonic acid. Arachidonic acid is metabolized (via lipoxygenase and cyclooxygenase) to prostaglandins and leukotrienes. These compounds play a role in the development of ischemia of the spinal cord following injury. 14 Increased intraneuronal sodium concentration induces cytotoxic edema and intracellular acidosis. 14 A decreased intracellular potassium concentration may modify the membrane potential (or resting potential), resulting in conduction failure of affected neurons. 17 The normal spinal cord is devoid of neutrophils and macrophages. Days to weeks after spinal cord injury, mixed neutrophilic macrophagic inflammation is evident at the site of spinal cord injury. In one study, giant macrophages were identified in the damaged spinal cord 3 days to 3 weeks following the initial injury. 18 Enzymes produced by neutrophils and macrophagic phagocytosis may further damage the neural tissue. This process produces cavitation within the gray and white matter (Figure 3). The resultant cavity is thought to act as a mechanical barrier, preventing axonal regeneration. 14 Histologic Findings and Clinical Implications As a result of a higher metabolic rate and oxygen demand, gray matter is more susceptible to ischemia than white matter. Therefore, both primary and secondary injuries initially affect the gray matter. Depending on the injuring force, gray matter histologic findings range from central petechial hemorrhages to severe hemorrhagic necrosis and cavitation (Figure 3). 10 In white matter, the histopathologic findings range from mild demyelination Figure 3A Acute spinal cord trauma Figure 3B Chronically affected spinal cord Figure 3 (A) Gross spinal cord cross-section from a dog with acute spinal cord trauma. A large focus of hemorrhage and malacia affecting the gray and white matter is noted. The bar on the ventral side of spinal cord represents 1 cm. (B) Microscopic cross-section of a chronically affected spinal cord. The cord is flattened, and there is a loss of normal architecture. The dorsal portion of the spinal cord is replaced by connective tissue (CT). The ventral part is misshapen and cavitated (C). Hematoxylin and eosin staining were used. The bar represents 0.5 cm. CC = central canal; M = meninges; VMF = ventral median fissure.
4 262 Small Animal/Exotics Compendium April 2003 to severe hemorrhagic necrosis with cavitation (Figure 3). 19 The pathology may propagate longitudinally to adjacent cord segments of white matter. This process may ultimately result in ascending descending diffuse myelomalacia. 20 Damage to gray and white matters in general is well established within 8 hours and most secondary mechanisms typically last for up to 48 hours following the initial injury. 21 Clinically, the severity of neurologic deficits correlates with the severity of the spinal cord damage. Deficits are first observed in conscious proprioception. Then, progressive loss of motor function, superficial pain, and finally deep pain sensation occur. 22 Patients with a minor injury of the spinal cord essentially limited to the gray matter and sparing the white matter may remain asymptomatic. Indeed, damage to the gray matter (unless a limb plexus is affected) has fewer clinical consequences than lesions of the white matter. 23 For example, if one selectively damages and destroys the gray matter at the level of T10, the only clinical consequence will be a loss of muscle tone in the area of the T10 myotome. However, the white matter containing all ascending and descending tracts will be structurally and functionally unaffected and hindlimb function will not be compromised. Diffuse Myelomalacia In some animals, following a severe concussive injury, the cascade of events continues, resulting in the progressive longitudinal extension of spinal cord pathology in both cranial and caudal directions (Figure 3). This process may occur over a few days following the initial spinal cord trauma and results in ascending descending diffuse myelomalacia. 24 Following a thoracolumbar disk herniation, this may be clinically characterized by systemic signs of toxemia, a flaccid abdomen, the level of cut-off of the cutaneous trunci reflex response migrating cranially, a shift from upper motor neuron to lower motor neuron signs in the rear limbs, neurologic deficits progressing to involve the forelimbs, and eventually respiratory paralysis. 25 A delay in the onset of ascending descending diffuse myelomalacia may result in clinical signs only becoming evident postoperatively. 7 Physical examination, myelography, and intraoperative findings help identify diffuse myelomalacia. The prognosis is poor, and death from respiratory paralysis is a common sequela. Euthanasia is often recommended to prevent further suffering. 25 Compressive Spinal Cord Trauma Following an intervertebral disk herniation, spinal cord compression may occur in two ways: as a result of a mass of disk material and hematoma pushing against the spinal cord (extradural compression) and by swelling of the spinal cord within the rigid dura mater (intramedullary compression). Extradural Compression Extradural spinal cord compression following a Hansen type II disk protrusion usually is associated with progressive compression of the spinal cord. However, a type I disk herniation may result in peracute compression of the spinal cord. The extruded nucleus pulposus and associated hematoma occupy the vertebral canal and comprise an extradural compressive mass. Experimentally, compression of the spinal cord has been studied by implantation of slow-growing tumors in the epidural space in rats. 26 Whereas concussive injury primarily affects the gray matter, slow gradual compressive injury mainly results in white matter pathology. Lesions range from demyelination to severe malacia, depending on the extent
5 Compendium April 2003 Spinal Cord Trauma: Pathophysiology 263 and rate of compression. 23 With mild compression, pain due to the irritation of nerve roots (radicular pain) and meninges (meningeal pain) is experienced first. Neurologic dysfunction occurs in a consistent and predictable order. The nerve fiber diameter determines the order in which neurologic deficits progress. 22 The large diameter fibers relaying proprioceptive information constitute the first tracts to be affected. The medium diameter fibers, responsible for motor function and superficial pain, are affected next. The small diameter nonmyelinated fibers responsible for deep pain sensation are the most resistant to injury and consequently the last to be affected by injury to the spinal cord. With progressive compression of the spinal cord, the animal may first show proprioceptive deficits and ataxia. The patient may then become nonambulatory and lose motor function. With severe compression, superficial and, finally, deep pain sensation are lost. 7,22 Intramedullary Compression The spinal cord, surrounded by an inextensible dura mater, may be further compressed by the presence of parenchymal swelling (intramedullary compression). Both edema and hemorrhage may result in spinal cord swelling following spinal cord injury. Experimental studies in dogs have demonstrated that intramedullary extravasation of blood proteins and associated edema is maximum following acute concussive injury (type I herniations) and minimal with compressive injury (type I and type II herniations). 19 However, experimentally, rapid decompression of the spinal cord also resulted in vascular leakage and edema. 19 It has been suggested that the edema is the result of reperfusion injury with free radical mediated damage to the endothelial cells of the spinal cord microvasculature. 16 Finally, a large extradural compressive mass may effectively obstruct the ventral venous sinuses, resulting in an elevation of the venous hydrostatic pressure. This, in turn, may precipitate intramedullary edema and swelling of the spinal cord. 16 In such conditions, progressive spinal cord pathology may worsen acutely after impairment of venous drainage. For instance, an atactic dog with a type I or type II disk herniation may become acutely paraplegic following obstruction of the venous sinuses. 16 SUMMARY Spinal cord injury following intervertebral disk herniation is a combination of concussive and compressive injury. Concussion of the spinal cord acutely damages meninges, blood supply, and neural tissue. This constitutes the primary injury. Following primary injury, a cascade of vascular, biochemical, and cellular events results in additional secondary injury to the spinal cord. Compression of the spinal cord following intervertebral disk herniation may result from a mass of herniated disk material and hematoma within the vertebral canal (extradural compression) or spinal cord swelling within a rigid dura mater (intramedullary compression). An uncommon sequela of spinal cord trauma is ascending descending diffuse myelomalacia. Knowledge and understanding of the pathophysiology are important for the diagnosis and treatment of spinal cord injury. REFERENCES 1. Bray JP, Burbidge HM: The canine intervertebral disk. JAAHA 34:55 63, , Anderson SM, Lippincott CL, Gill PJ: Hemilaminectomy in dogs without deep pain perception. Calif Vet 45(5):24 28, Borgens RB, Toombs JP, Blight AR, et al: Effects of applied electric fields on clinical cases of complete paraplegia in dogs. Restorative Neurol Neurosci 5: , Scott HM, McKee WM: Laminectomy for 31 dogs with thoracolumbar disk disease and loss of deep pain perception. J Small Anim Pract 40: , Puerto DA, Laitinen OM, Kapatkin AS: Surgical decompression in dogs with thoracolumbar intervertebral disk disease and loss of deep pain perception: A retrospective analysis of 47 cases. Vet Surg 29(5):473, Shores A: Spinal trauma. Pathophysiology and management of traumatic spinal injuries. Vet Clin North Am Small Anim Pract 22(4): , Toombs JP, Bauer MS: Intervertebral disc disease, in Slatter D (ed): Textbook of Small Animal Surgery, vol 1. Philadelphia, WB Saunders, 1993, pp Braund KG: Acute spinal cord trauma, in Bojrab JM (ed): Disease Mechanisms in Small Animal Surgery. Philadelphia, Lea & Febiger, 1993, pp Ichihara K, Taguchi T, Shimada Y, et al: Gray matter of the bovine cervical spinal cord is mechanically more rigid and fragile than the white matter. J Neurotrauma 18(3):361 67, Griffiths IR: Some aspects of the pathology and pathogenesis of the myelopathy caused by disc protrusions in the dog. J Neurol Neurosurg Psychiatry 35: , Guha A, Tator CH: Acute cardiovascular effects of experimental spinal cord injury. J Trauma 28: , Griffiths IR, Trench JG, Crawford RA: Spinal cord blood flow and conduction during experimental cord compression in normotensive and hypotensive dogs. J Neurosurg 50(3): , Hall ED, Wolf DL: A pharmacological analysis of the pathophysiological mechanisms of posttraumatic spinal cord ischemia. J Neurosurg 64(6): , Dumont RJ, Okonkwo DO, Verma S: Acute spinal cord injury. Part 1: Pathophysiologic mechanisms. Clin Neuropharmacol 24(5): , Brown SA, Hall ED: Role of oxygen-derived free radicals in the
6 264 Small Animal/Exotics Compendium April 2003 pathogenesis of shock and trauma, with focus on central nervous system injuries. JAVMA 200(12): , Hall ED, Braughler JM: Central nervous system trauma and stroke. II. Physiological and pharmacological evidence for involvement of oxygen radicals and lipid peroxidation. Free Radic Biol Med 6: , Berg JR, Rucker NC: Pathophysiology and medical management of acute spinal cord injury. Compend Contin Educ Pract Vet 7(8): , Leskovar A, Turek J, Borgens RB: Giant multinucleated macrophages occur in acute spinal cord injury. Cell Tissue Res 304: , Griffiths IR: Vasogenic edema following acute and chronic spinal cord compression in the dog. J Neurosurg 42: , Salisbury SK, Cook JR: Recovery of neurological function following focal myelomalacia in a cat. JAAHA 24(2): , Olby NJ: Current concepts in the management of spinal cord injury. J Vet Intern Med , Lorentz MD, Oliver JE, Kornegay JN: Handbook of Veterinary Neurology, ed 3. Philadelphia, WB Saunders, 1993, p Vandevelde M, Wolf M: Spinal cord compression, in Bojrab JM (ed): Disease Mechanisms in Small Animal Surgery. Philadelphia, Lea & Febiger, 1993, pp Griffiths IR: The extensive myelopathy of intervertebral disc protrusion in dogs ( the ascending syndrome ). J Small Anim Pract 13: , Wheeler SJ, Sharp NJH: Small Animal Spinal Disorders: Diagnosis and Surgery. London, Mosby-Wolfe, Kato A: Circulatory disturbance of the spinal cord with epidural neoplasms in rats. J Neurosurg 63: , ARTICLE #1 CE TEST The article you have read qualifies for 1.5 contact hours of Continuing Education Credit from the Auburn University College of Veterinary Medicine. Choose the best answer to each of the following questions; then mark your answers on the postage-paid envelope inserted in Compendium. 1. What is the primary injury following intervertebral disk herniation? a. trauma to the spinal cord and meninges b. electrolytes changes c. free radical production d. spinal cord swelling 2. In normal animals, a mild decrease in the systemic blood pressure is followed by a. a drop in the spinal cord perfusion. b. no change in the spinal cord perfusion. c. an increase in spinal cord blood flow. d. a phase of systemic hypertension. 3. Following spinal cord injury, massive production of free radicals leads to a. the peroxidation of membrane phospholipids. b. electrolyte abnormalities in the spinal cord cytosol. c. microvasculature damage. d. all of the above 4. Which mechanism contributes to the formation of an area of cavitation within the injured spinal cord? a. vascular damage b. neutrophil- and macrophage-mediated damage c. primary injury d. meningeal damage 5. In most cases, the cascade of events may last up to 48 hours following spinal cord injury. However, in some cases, the cascade does not stop, leading to a. ascending descending diffuse myelomalacia. b. focal myelomalacia. c. white matter damage only. d. gray matter damage only. 6. What ion(s) massively enters the neuronal cytosol following spinal cord injury? a. calcium b. potassium c. sodium d. sodium and calcium 7. Potassium ions efflux after spinal cord injury leads to a. conduction failure. b. neuronal autolysis. c. change in neuronal membrane potential. d. a and c 8. What is the clinical implication of a selective destruction of the gray matter at the level of T10? a. none b. paraplegia and loss of deep pain perception c. decreased muscle tone in the T10 myotome d. increased intracranial pressure 9. Spinal cord swelling may be caused by a. spinal cord edema and intramedullary hemorrhages. b. acute decompression of the spinal cord. c. compression of the venous sinuses. d. all of the above 10. With progressive compression of the spinal cord, which fibers are the first to be affected? a. the fibers carrying the proprioceptive information b. the larger-diameter fibers c. a and b d. the fibers located most superficially
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