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© 1997 The Journal of Bone and Joint Surgery, Inc. The Ankle Clonus Test for Assessment of the Integrity of the Spinal Cord during Operations for Scoliosis*   Investigation performed at the Jack D. Weiler Hospital of the Albert Einstein College of Medicine, a Division of Montefiore Hospital and Medical Center, Bronx
The ankle clonus test, a method for evaluating the integrity of the spinal cord during operations for scoliosis, is predicated on the finding that patients recovering from general anesthesia normally have temporary ankle clonus bilaterally. An absence of transient ankle clonus has been shown to indicate neurological compromise. The test was performed for 1006 patients who were being managed with spinal arthrodesis and instrumentation and 115 control patients who had an operation under general anesthesia because of a condition that was unrelated to the spine. The six patients in whom a neurological deficit developed all had had a so-called positive result on the ankle clonus test (that is, an absence of transient ankle clonus). There were no false-negative results and three false-positive results; the test therefore had a sensitivity of 100 per cent and a specificity of 99.7 per cent. The ankle clonus test was found to be more accurate than the wake-up test and monitoring of somatosensory evoked potentials for predicting neurological compromise.
Injury of the spinal cord and the nerve roots is a dreaded complication of the use of spinal instrumentation for the treatment of scoliosis. In a combined study that was published in 1987, the Morbidity and Mortality Committee of the Scoliosis Research Society reported that the prevalence of this complication was 0.62 per cent (five of 805 patients)10. Although this prevalence is relatively low, a neurological injury is a potentially catastrophic complication for the individual who is affected. Such an injury can occur as the result of either traction palsy or ischemia when distraction is applied to the concave side of a curve. In patients who have a flexible idiopathic curve, neurological compromise is thought to be due to disruption of the vasculature of the spinal cord. Dommisse described a so-called critical vascular zone (from approximately the fourth to the ninth thoracic vertebra) in which the blood supply to the anterior portion of the spinal cord is poorest and the spinal canal is narrowest. Thus, the region in which an arthrodesis commonly is performed for the treatment of scoliosis is the region in which the blood supply to the spinal cord is most tenuous. Ponte supported the concept of an ischemic etiology when he described the cases of two patients in whom paraplegia associated with hypovolemia resolved with correction of the low blood volume. Paraplegia more commonly is associated with the correction of congenital curves12. In these instances, the neurological injury probably occurs secondary to tethering of the spinal cord or the nerve roots or to avulsion of the latter. Such an injury may be avoided with careful operative planning and meticulous operative technique and seldom results from direct trauma during decortication and the placement of hooks. The decision regarding the amount of correction to be attempted and accepted relies heavily on the clinical judgment of the surgeon. To assist in this decision and to allow greater amounts of correction to be achieved safely, several methods for the intraoperative evaluation of the integrity of the spinal cord have been proposed. Vauzelle et al., in 1973, described the so-called wake-up test, which is now used widely5,6. The disadvantage of the wake-up test is that it requires the patient to be awakened fully, which potentially disrupts the sterile operative field and may jeopardize the airway of the patient. Furthermore, the test is crude: it is used to evaluate gross movement only and cannot be used to evaluate fine motor function. Continuous intraoperative monitoring of somatosensory evoked potentials, as advocated by Engler et al. and Nash et al., also is used widely. This technique, however, is employed only to monitor signal conduction in the sensory columns of the spinal cord. These tracts are concentrated posteromedially and thus are away from the anterior aspect of the spinal cord, where the vascular insult generally occurs. Moreover, as changes in the anterior horn cells may result in changes in somatosensory evoked potentials, a spinal cord injury may be missed with this technique. There are, of course, sensory signals that are carried more anteriorly, in the lateral spinothalamic tracts. Because of this, and because most injuries are not confined entirely to the anterior corticospinal tracts, monitoring of somatosensory evoked potentials usually is an effective technique1. Nevertheless, the potential exists for a spinal cord injury to be missed as the result of observer error or failure of the technique to detect an injury that is confined anteriorly7. The purpose of the present report is to describe our experience with the ankle clonus test, which we found to be a safe and reliable means of assessing the integrity of the spinal cord—including the anterior columns (the anterior corticospinal tracts)—during operations for scoliosis. The ankle clonus reflex is assessed by performing a rapid forced dorsiflexion of the foot and then holding slight tension on the foot in the dorsiflexed position. Rhythmic contractions of the gastrocnemius muscle resulting in plantar flexion of the foot indicate a normal response. The clonus reflex is not found in a normal, awake patient. It was described by Dimitrejevic et al. as a "hyper-reflexic state often associated with spasticity and upper motor neuron lesions. It is a series of rhythmic contractions of muscle at a frequency of five to seven hertz in response to an abruptly and continuously applied stretch reflex." The clonus reflex requires an intact spinal stretch reflex and sustained hyperexcitability of the lower motor neurons secondary to a loss of central inhibition. In the case of the ankle clonus reflex, the first sacral nerve root mediates the spinal stretch reflex arc. The ankle clonus test is predicated on the finding that patients recover from general anesthesia in stages. Lower-motor-neuron function returns first, with inhibitory (cortical) impulses returning later. This situation produces an initial imbalance in which the lower motor neurons are not inhibited; thus, clonus may be elicited early during the reversal of anesthesia, when the patient still is unable to move and is unresponsive to verbal stimuli. Ankle clonus is present at this stage until inhibitory impulses from the motor cortex of the brain override excitatory impulses. If there is an injury of the spinal cord, spinal shock causes a diminution of lower-motor-neuron impulses, resulting in a loss of the ability to produce ankle clonus. Similarly, as anesthesia is being administered, inhibitory (cortical) impulses are lost first, resulting in a relatively excitatory state of the lower motor neurons and the appearance of ankle clonus, which disappears when a deeper level of anesthesia is achieved.
The present study included 1121 patients who were managed at the Jack D. Weiler Hospital of the Albert Einstein College of Medicine, a Division of Montefiore Medical Center, from April 1976 to January 1994. Of these patients, 842 had Harrington-rod instrumentation and arthrodesis, 164 had Cotrel-Dubousset instrumentation and arthrodesis, and 115 served as controls. Most of the patients in the two study groups had the operation because of scoliosis, but nine had it because of a spinal fracture or a degenerative condition involving the lumbar spine. The patients in the control group were randomly selected, neurologically normal patients who had ophthalmological, gynecological, or urological procedures that did not place the spinal cord at risk (Table I).
The ankle clonus test was performed in the surgeon's office as part of the preoperative neurological assessment as well as in the operating room before the induction of anesthesia. None of the 958 patients who had idiopathic scoliosis had ankle clonus preoperatively, compared with seventeen of the twenty-two patients who had neuromuscular scoliosis. The first 715 patients also were tested for ankle clonus repetitively during the induction of anesthesia; all had bilateral ankle clonus while under light anesthesia, at which time excitatory impulses exceeded inhibitory ones. Ankle clonus disappeared when a deeper state of anesthesia was achieved. The remaining 406 patients were not evaluated during the induction of anesthesia because our findings had been confirmed in the first group; anesthesia therefore was induced rapidly for these patients. Initially, anesthesia was induced by the intravenous administration of sodium pentothal along with a muscle relaxant, followed by the administration of a combination of the inhalational agents nitrous oxide and halothane. Later in the study, halothane was replaced with isoflurane. After distraction or correction of the curve, the anesthesiologist was instructed to lighten the level of anesthesia. It is at this time that the wake-up test customarily is performed. During this process, the patients who had been managed with spinal arthrodesis were tested repeatedly for bilateral ankle clonus. Muscle tone increases gradually; the clonus test must be performed as the tone increases so that the reflex is not missed. Ankle clonus was expected to appear early, during the period in which excitatory impulses exceed inhibitory ones. Absence of the reflex, either unilaterally or bilaterally, indicated a change in the function of the spinal cord. If the reflex was absent, a wake-up test was performed. The control patients also were evaluated with regard to the presence of ankle clonus during the reversal of anesthesia. A Stagnara wake-up test was performed in addition to the ankle clonus test for the 415 patients who were managed before 1984. Beginning in 1984, intraoperative monitoring of somatosensory evoked potentials was performed in addition to the ankle clonus test and, in general, instead of the wake-up test.
Seventeen patients (all of whom had neuromuscular scoliosis) had ankle clonus before the induction of anesthesia, and all 715 patients who were evaluated during induction had ankle clonus bilaterally while under light anesthesia. Over-all, nine patients had an absence of ankle clonus with reversal of anesthesia: four patients who had been managed with Harrington-rod instrumentation and one who had been managed with Cotrel-Dubousset instrumentation had unilateral absence of ankle clonus, and three patients who had been managed with Harrington-rod instrumentation and one who had been managed with Cotrel-Dubousset instrumentation had bilateral absence. None of the patients who had a normal result on the ankle clonus test demonstrated any neurological deficit. The three patients who had bilateral absence of ankle clonus after Harrington-rod instrumentation also did not demonstrate any evidence of neurological deficit; therefore, the results of the test were false-positive for these patients. The other six patients in whom ankle clonus was absent all had some form of neurological deficit (Table II).
The first such patient was a thirteen-year-old girl who had Harrington-rod instrumentation because of idiopathic scoliosis. Somatosensory evoked potentials were normal throughout the procedure, and the result of the wake-up test was normal as well. Ankle clonus was absent unilaterally with reversal of anesthesia. Eight hours postoperatively, the patient had weakness of the extensors of the toes on the side on which ankle clonus had been absent. This deficit gradually resolved after immediate removal of the instrumentation. The patient was managed effectively with a body cast. The second patient also was a thirteen-year-old girl who had Harrington-rod instrumentation because of idiopathic scoliosis. Ankle clonus was absent unilaterally after distraction. Movement of all four limbs was grossly intact during the wake-up test. Weakness on one side of the body and sensory changes in the contralateral lower extremity were noted when the patient was fully awake; these findings were consistent with a Brown-Séquard syndrome. The patient was managed with immediate removal of the instrumentation. The neurological deficit resolved completely within two weeks. Partial correction was maintained with a Risser localizer cast. The third patient was an eighteen-year-old man who had bilateral Harrington-rod instrumentation with distraction because of a burst fracture of the fifth lumbar vertebra. Ankle clonus was absent unilaterally after instrumentation. Gross movement of all four limbs was noted on the wake-up test. In the recovery room, the patient was found to have weakness of the gastrocnemius muscle as well as diminished sensation in the first sacral dermatome on the side on which ankle clonus had been absent. The instrumentation was left in place, and the deficits resolved completely before the patient was discharged from the hospital. The fourth patient was a twelve-year-old girl with congenital scoliosis who was managed with Harrington-rod instrumentation without distraction after an uneventful period of halo-pelvic traction in the hospital. Ankle clonus was absent on the right side immediately after instrumentation. Markedly decreased movement of the ipsilateral lower extremity was noted on the wake-up test. Since no distraction had been applied, the rods were left in place. Complete paralysis of the right lower extremity was noted when the patient was fully awake and alert. The patient immediately was taken to the operating room for removal of the instrumentation and exploration of the dural sac, but the findings were normal. The neurological deficit did not resolve. The fifth patient was a fourteen-year-old boy who was managed with Cotrel-Dubousset instrumentation because of idiopathic scoliosis. A sudden change in somatosensory evoked potentials in the left lower extremity and an absence of ankle clonus on the ipsilateral side were noted after spinal correction. The findings of the wake-up test were normal, as were those of a postoperative neurological examination. Approximately sixteen hours later, however, the patient was noted to have weakness of the extensor hallucis longus as well as a sensory deficit in the fifth lumbar dermatome. The instrumentation was not removed, and the patient recovered fully. Although gross motor function was intact on the wake-up test, the absence of ankle clonus and the sudden change in somatosensory evoked potentials predicted this deficit. The sixth patient was a thirteen-year-old girl who was managed with Cotrel-Dubousset instrumentation because of idiopathic scoliosis. Somatosensory evoked potentials were normal throughout the procedure, but ankle clonus was absent bilaterally after instrumentation. Postoperatively, the patient was observed closely because of the absence of ankle clonus. Within one hour, she was noted to have hyperreflexia of the lower extremities as well as sustained bilateral ankle clonus. She was returned to the operating room for removal of the instrumentation. Reflexes then returned to normal. A Risser localizer cast subsequently was applied to maintain correction. Four of these patients had a normal result on the intraoperative wake-up test. All four had an abnormal result on the ankle clonus test as well as postoperative neurological deficits. The twenty-two patients who had neuromuscular scoliosis all had a normal result on the ankle clonus test with reversal of anesthesia; this group included the seventeen patients who had had ankle clonus before the induction of anesthesia. The 115 control patients all had bilateral ankle clonus with slow induction of anesthesia and again with reversal of anesthesia. There were no false-negative results and three false-positive results; the ankle clonus test therefore had a sensitivity of 100 per cent and a specificity of 99.7 per cent.
The ankle clonus test is an important addition to the techniques for monitoring function of the spinal cord after spinal instrumentation and correction. Its advantage compared with the Stagnara wake-up test is that it does not require the patient to be awakened fully, which potentially disrupts the sterile operative field and the airway of the patient. Moreover, the wake-up test may require more than fifteen minutes whereas the ankle clonus test requires only a lightened state of anesthesia. The ankle clonus test also has an advantage compared with monitoring of somatosensory evoked potentials (which is used mainly to assess the posterior columns of the spinal cord) in that it allows the integrity of the anterior columns to be evaluated as well. The present study demonstrated that the ankle clonus test is a highly accurate gauge of the integrity of the spinal cord; there were no false-negative results and only three false-positive results—three patients who were managed with Harrington-rod instrumentation had an absence of ankle clonus bilaterally but had no neurological deficit. It is possible that ankle clonus was not apparent in these three patients because they had awakened from anesthesia too rapidly, which may have shortened the period during which excitatory impulses exceeded inhibitory ones. Ankle clonus therefore may have been missed by the examiner. A positive result on the ankle clonus test (that is, the absence of clonus) predicted the neurological deficit in all six patients in whom such a complication developed. Three of these patients had been managed with Harrington-rod instrumentation during the earlier part of the study, before the use of monitoring of somatosensory evoked potentials. Of these patients, only one (a twelve-year-old girl in whom complete paralysis of the right lower extremity developed) had an abnormal result on the wake-up test. One other patient who had a neurological deficit after Harrington-rod instrumentation had a negative result both on the wake-up test and on monitoring of somatosensory evoked potentials. The other two patients in whom a neurological deficit developed had been managed with Cotrel-Dubousset instrumentation and had been assessed with monitoring of somatosensory evoked potentials, but that method of evaluation indicated dysfunction in only one. Several important findings emerged from our experience with the ankle clonus test. For the result of the test to be considered normal, transient bilateral clonus must be elicited with reversal of anesthesia. Ankle clonus often returns asymmetrically—that is, it appears on one side before it appears on the other. It is not the number of beats of clonus that is important but rather the presence or absence of the finding. Also, ankle clonus may not be apparent at the start of the procedure if anesthesia is induced rapidly. Patients who have an absence of ankle clonus despite normal findings on monitoring of somatosensory evoked potentials and on the wake-up test must be observed closely in the recovery room because the absence of clonus may be a precursor of neurological compromise. Furthermore, patients who have ankle clonus before the induction of anesthesia should have a return of ankle clonus with reversal of anesthesia as an indication that baseline function of the spinal cord is intact. Admittedly, it is difficult to rely on the return of an abnormal neurological state to ascertain that no injury of the spinal cord has occurred, and this makes the utility of this test less certain for patients who have preoperative ankle clonus. We also found that ankle clonus can recur in the recovery room shortly after the administration of a narcotic; this finding is normal when temporary. The ankle clonus test is a safe, sensitive, accurate, and easily performed method for the intraoperative assessment of the integrity of the spinal cord. The test ideally is performed immediately after spinal instrumentation, and that is our current protocol. We believe that if the result of the ankle clonus test is abnormal, a wake-up test should be performed to confirm the presence of a neurological deficit. This recommendation is made in view of the fact that there were three false-positive results in the present study. We do not wish to relax the instrumentation or remove it without first attempting to confirm the abnormal findings. We do not perform a wake-up test if the result of the ankle clonus test is normal. Whenever possible, the ankle clonus test is used in conjunction with monitoring of somatosensory evoked potentials in order to ensure maximum safety. The test is repeated at the termination of the procedure as a final assessment of neurological function before the patient is awakened fully.
*No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. No funds were received in support of this study.
¶Department of Orthopaedic Surgery, Long Island Jewish Medical Center/Schneider Children's Hospital, New Hyde Park, New York 11040.
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