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Peripheral neurophysiology of acute distal spinal cord infarction
Peripheral Neurophysiology of Acute Distal Spinal Cord Infarction Steven H. Horowitz, MD, and Nitin Patel, MD F-wave abnormalities, in the presence of normal distal motor nerve conduction, most often are the first indicators of proximal peripheral nerve dysfunction in demyelinating polyradiculoneuropathies. However, a 15-year-old female—who developed lumbosacral spinal cord infarction with paraplegia, sensory loss, and incontinence beginning 15 hours after a fall—studied electrophysiologically at 2 days postparaplegia manifested absent lower-extremity f-waves and H-reflexes and normal compound muscle action potentials and distal motor and sensory conduction velocities. Subsequent evaluations demonstrated permanent loss of compound muscle action potentials, f-waves, and Hreflexes and prominent acute denervation in paralyzed lower-extremity muscles. Thus early f-wave and Hreflex loss can also occur in spinal cord disease, thereby representing the first evidence of motoneuron destruction. © 2003 by Elsevier Science Inc. All rights reserved. Horowitz SH, Patel N. Peripheral neurophysiology of acute distal spinal cord infarction. Pediatr Neurol 2003;28: 64-65.
Introduction In rapidly progressive paraparesis, early loss of f-waves and H-reflexes with simultaneous preserved compound muscle action potentials and distal motor conduction velocities in lower-extremity nerves usually indicates acute inflammatory demyelinating polyneuropathy. A rare
From the Division of Neurology, University of Missouri School of Medicine Columbia, Missouri.
64
PEDIATRIC NEUROLOGY
Vol. 28 No. 1
and difficult-to-diagnose alternative etiology is distal spinal cord pathology [1]. We report a 15-year-old patient with acute lumbosacral cord infarction, paraplegia, and these early neurophysiologic features after a fall. Subsequently, permanent loss of these late motor responses and compound muscle action potentials developed. Case Report A 15-year-old female fell directly on her buttocks while ballet dancing. She continued to dance and walked home afterward. The next morning (about 15 hours later), her movements were unsteady when she arose; within 15 minutes she developed paraplegia, lower-extremity numbness, and bowel and bladder incontinence. On admission to the hospital, she had flaccid paraplegia, absent lower-extremity reflexes, loss of all sensation distal to L2, and no anal tone or wink, and she required bladder catheterization. At repeated examinations from 7 to 15 months, there was paraplegia with substantial wasting of all lower-extremity muscles, minimal and patchy return of only vibratory and proprioceptive sensations below L3, areflexia, and no bowel or bladder control. Beginning 3 days postparaplegia, magnetic resonance imaging revealed infarction of the lumbosacral spinal cord and conus medullaris (Fig 1). Conduction studies of lower-extremity motor (both peroneal and posterior tibial) and sensory (left sural and superficial peroneal) nerves were performed 2 days, 2 weeks, and 3 and 7 months postparaplegia. At 2 days, there were absent f-waves and H-reflexes, with normal sensory and motor velocities and sensory nerve action potential and compound muscle action potential amplitudes. Electromyographic studies were deferred. At each evaluation thereafter, compound muscle action potentials, f-waves, and H-reflexes were absent, sensory-study results were normal, and electromyography revealed prominent diffuse acute denervation, without voluntary motor unit potentials, in all lower-extremity muscles; the paraspinal muscles were normal. Additionally, at 7 months isolated voluntary polyphasic motor unit potentials were present in the right vastus medialis, as was a prolonged femoral nerve latency to that muscle (8.3 ms), with a compound muscle action potential of extremely low amplitude (0.2 mv). Evoked potential studies revealed mild delays in P37 and N43 waves bilaterally.
Discussion This patient manifested a lumbosacral spinal cord infarction, mainly in the distribution of the anterior spinal artery. Included within its watershed are anterior horn motoneurons. Complete and permanent flaccid paralysis in the lower extremities with atonic bowel and bladder and areflexia indicates bilateral motoneuron damage from L2 distally. This indication was corroborated neuroradiologically (Fig 1). In the lumbosacral area the anterior spinal artery receives blood via the artery of Adamkiewicz [2]. Although spinal angiography was not performed, the delayed onset of neurologic symptoms suggests gradual
Communications should be addressed to: Dr. Patel; Division of Neurology; University of Missouri School of Medicine, Columbia; MO 65212. Received May 15, 2002; accepted June 11, 2002.
© 2003 by Elsevier Science Inc. All rights reserved. doi:10.1016/S0887-8994(02)00495-2 ● 0887-8994/03/$—see front matter
Figure 1. T2 (TR/TE 420/140.0/1)–weighted sagittal magnetic resonance imaging 2 weeks after onset of paraplegia illustrating a high signal intensity indicative of infarction in the lumbosacral spinal cord and conus medullaris.
occlusion of arterial flow, perhaps secondary to a dissection of the artery of Adamkiewicz in its intervertebral foramen, initiated by vertical forces during the fall. F-waves, late motor responses generated by antidromic activation of spinal motoneurons, are helpful in assessing proximal peripheral nerve function in early acute inflammatory demyelinating polyneuropathy when distal motor nerve conduction may be normal [3]. They depend on the integrity of the motoneuron pool [3,4]. In spinal cord trauma or acute transverse myelitis, f-waves disappear below the level of injury during spinal shock and reappear with its resolution [4 – 6]. H-reflexes also depend on the motoneuron pool; they disappear in the first 24 hours of spinal shock but return thereafter [5]. In this patient, f-waves and H-reflexes were absent 2 days after onset of paraplegia when compound muscle action potentials and distal motor conduction were normal. The findings are comparable with those seen within the first 4 to 5 days postaxonotmesis, before Wallerian degen-
eration becomes manifest; distal compound muscle action potentials are demonstrable [7] and do not reflect the severity of injury. In this early stage, f-wave and H-reflex loss may be the only electrophysiologic evidence of neuronal damage. Although it is much more common to observe these electrophysiologic findings in paraparesis caused by inflammatory polyradiculoneuropathies with proximal conduction abnormalities, in this patient they occurred with damage to motoneurons in the spinal cord. The normal sensory nerve action potential amplitudes and sensory conduction reflect survival of dorsal root ganglia and argue against a peripheral nerve disorder. Continued absence of f-waves and H-reflexes with subsequent disappearance of compound muscle action potentials indicates complete and permanent loss of motoneurons at distal spinal cord levels. In cervical spinal cord injury, Curt et al. [4] found that f-wave production and compound muscle action potential amplitude relate to the severity and extent of damage to the segmental motoneuron pool. If compound muscle action potentials remain recordable, some portion of the motoneuron pool is viable; then if f-waves are absent, spinal shock is present and f-waves will return after its cessation. Spinal shock did not occur in this case, as witnessed clinically by the continuous flaccidity and loss of reflexes and electrophysiologically by loss of all measures of motor nerve activity; motoneurons themselves were damaged. Thus paraparesis or paraplegia and early and permanent loss of f-waves and H-reflexes in lower-extremity nerves may occur, although rarely, in primary distal spinal cord disorders. References [1] DeSeze J, Stojkovic T, Berteau G, et al. Acute myelopathies: Clinical, laboratory and outcome profiles in 79 cases. Brain 2001;124: 1509-21. [2] Crock HV, Yamagishi M, Crock MC. The arteries of the cauda equina and conus medullaris in man. In: The conus medullaris and cauda equina in man: An atlas of the arteries and veins. Vienna: SpringerVerlag, 1986;2-3, 9. [3] Fisher MA. AAEM minimonograph #13: H reflexes and f waves: Physiology and clinical considerations. Muscle Nerve 1992;15: 1223-33. [4] Curt A, Keck ME, Dietz V. Clinical value of f-wave recordings in traumatic cervical spinal cord injury. Electroenceph Clin Neurophysiol 1997;105:189-93. [5] Leis AA, Kronenberg MF, Stetkarova I, Paske WC, Stokic DS. Spinal motoneuron excitability after acute spinal cord injury in humans. Neurology 1996;47:231-37. [6] Marras C, Midroni G. Transient absence of f-waves in acute myelopathy: a potential source of diagnostic error. Electromyogr Clin Neurophysiol 2000;40:109-112. [7] Kimura J. Anatomy and physiology of peripheral nerve. In: Electrodiagnosis in diseases of nerve and muscle: Principles and practice, 3rd ed, 2001. New York: Oxford University Press, 75-90.
Horowitz and Patel: F-Wave and H-Reflex Loss in Spinal Infarction 65
Introduction In rapidly progressive paraparesis, early loss of f-waves and H-reflexes with simultaneous preserved compound muscle action potentials and distal motor conduction velocities in lower-extremity nerves usually indicates acute inflammatory demyelinating polyneuropathy. A rare
From the Division of Neurology, University of Missouri School of Medicine Columbia, Missouri.
64
PEDIATRIC NEUROLOGY
Vol. 28 No. 1
and difficult-to-diagnose alternative etiology is distal spinal cord pathology [1]. We report a 15-year-old patient with acute lumbosacral cord infarction, paraplegia, and these early neurophysiologic features after a fall. Subsequently, permanent loss of these late motor responses and compound muscle action potentials developed. Case Report A 15-year-old female fell directly on her buttocks while ballet dancing. She continued to dance and walked home afterward. The next morning (about 15 hours later), her movements were unsteady when she arose; within 15 minutes she developed paraplegia, lower-extremity numbness, and bowel and bladder incontinence. On admission to the hospital, she had flaccid paraplegia, absent lower-extremity reflexes, loss of all sensation distal to L2, and no anal tone or wink, and she required bladder catheterization. At repeated examinations from 7 to 15 months, there was paraplegia with substantial wasting of all lower-extremity muscles, minimal and patchy return of only vibratory and proprioceptive sensations below L3, areflexia, and no bowel or bladder control. Beginning 3 days postparaplegia, magnetic resonance imaging revealed infarction of the lumbosacral spinal cord and conus medullaris (Fig 1). Conduction studies of lower-extremity motor (both peroneal and posterior tibial) and sensory (left sural and superficial peroneal) nerves were performed 2 days, 2 weeks, and 3 and 7 months postparaplegia. At 2 days, there were absent f-waves and H-reflexes, with normal sensory and motor velocities and sensory nerve action potential and compound muscle action potential amplitudes. Electromyographic studies were deferred. At each evaluation thereafter, compound muscle action potentials, f-waves, and H-reflexes were absent, sensory-study results were normal, and electromyography revealed prominent diffuse acute denervation, without voluntary motor unit potentials, in all lower-extremity muscles; the paraspinal muscles were normal. Additionally, at 7 months isolated voluntary polyphasic motor unit potentials were present in the right vastus medialis, as was a prolonged femoral nerve latency to that muscle (8.3 ms), with a compound muscle action potential of extremely low amplitude (0.2 mv). Evoked potential studies revealed mild delays in P37 and N43 waves bilaterally.
Discussion This patient manifested a lumbosacral spinal cord infarction, mainly in the distribution of the anterior spinal artery. Included within its watershed are anterior horn motoneurons. Complete and permanent flaccid paralysis in the lower extremities with atonic bowel and bladder and areflexia indicates bilateral motoneuron damage from L2 distally. This indication was corroborated neuroradiologically (Fig 1). In the lumbosacral area the anterior spinal artery receives blood via the artery of Adamkiewicz [2]. Although spinal angiography was not performed, the delayed onset of neurologic symptoms suggests gradual
Communications should be addressed to: Dr. Patel; Division of Neurology; University of Missouri School of Medicine, Columbia; MO 65212. Received May 15, 2002; accepted June 11, 2002.
© 2003 by Elsevier Science Inc. All rights reserved. doi:10.1016/S0887-8994(02)00495-2 ● 0887-8994/03/$—see front matter
Figure 1. T2 (TR/TE 420/140.0/1)–weighted sagittal magnetic resonance imaging 2 weeks after onset of paraplegia illustrating a high signal intensity indicative of infarction in the lumbosacral spinal cord and conus medullaris.
occlusion of arterial flow, perhaps secondary to a dissection of the artery of Adamkiewicz in its intervertebral foramen, initiated by vertical forces during the fall. F-waves, late motor responses generated by antidromic activation of spinal motoneurons, are helpful in assessing proximal peripheral nerve function in early acute inflammatory demyelinating polyneuropathy when distal motor nerve conduction may be normal [3]. They depend on the integrity of the motoneuron pool [3,4]. In spinal cord trauma or acute transverse myelitis, f-waves disappear below the level of injury during spinal shock and reappear with its resolution [4 – 6]. H-reflexes also depend on the motoneuron pool; they disappear in the first 24 hours of spinal shock but return thereafter [5]. In this patient, f-waves and H-reflexes were absent 2 days after onset of paraplegia when compound muscle action potentials and distal motor conduction were normal. The findings are comparable with those seen within the first 4 to 5 days postaxonotmesis, before Wallerian degen-
eration becomes manifest; distal compound muscle action potentials are demonstrable [7] and do not reflect the severity of injury. In this early stage, f-wave and H-reflex loss may be the only electrophysiologic evidence of neuronal damage. Although it is much more common to observe these electrophysiologic findings in paraparesis caused by inflammatory polyradiculoneuropathies with proximal conduction abnormalities, in this patient they occurred with damage to motoneurons in the spinal cord. The normal sensory nerve action potential amplitudes and sensory conduction reflect survival of dorsal root ganglia and argue against a peripheral nerve disorder. Continued absence of f-waves and H-reflexes with subsequent disappearance of compound muscle action potentials indicates complete and permanent loss of motoneurons at distal spinal cord levels. In cervical spinal cord injury, Curt et al. [4] found that f-wave production and compound muscle action potential amplitude relate to the severity and extent of damage to the segmental motoneuron pool. If compound muscle action potentials remain recordable, some portion of the motoneuron pool is viable; then if f-waves are absent, spinal shock is present and f-waves will return after its cessation. Spinal shock did not occur in this case, as witnessed clinically by the continuous flaccidity and loss of reflexes and electrophysiologically by loss of all measures of motor nerve activity; motoneurons themselves were damaged. Thus paraparesis or paraplegia and early and permanent loss of f-waves and H-reflexes in lower-extremity nerves may occur, although rarely, in primary distal spinal cord disorders. References [1] DeSeze J, Stojkovic T, Berteau G, et al. Acute myelopathies: Clinical, laboratory and outcome profiles in 79 cases. Brain 2001;124: 1509-21. [2] Crock HV, Yamagishi M, Crock MC. The arteries of the cauda equina and conus medullaris in man. In: The conus medullaris and cauda equina in man: An atlas of the arteries and veins. Vienna: SpringerVerlag, 1986;2-3, 9. [3] Fisher MA. AAEM minimonograph #13: H reflexes and f waves: Physiology and clinical considerations. Muscle Nerve 1992;15: 1223-33. [4] Curt A, Keck ME, Dietz V. Clinical value of f-wave recordings in traumatic cervical spinal cord injury. Electroenceph Clin Neurophysiol 1997;105:189-93. [5] Leis AA, Kronenberg MF, Stetkarova I, Paske WC, Stokic DS. Spinal motoneuron excitability after acute spinal cord injury in humans. Neurology 1996;47:231-37. [6] Marras C, Midroni G. Transient absence of f-waves in acute myelopathy: a potential source of diagnostic error. Electromyogr Clin Neurophysiol 2000;40:109-112. [7] Kimura J. Anatomy and physiology of peripheral nerve. In: Electrodiagnosis in diseases of nerve and muscle: Principles and practice, 3rd ed, 2001. New York: Oxford University Press, 75-90.
Horowitz and Patel: F-Wave and H-Reflex Loss in Spinal Infarction 65