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Show Journal of Neuro- Oplilliiilniohi. Ky I9( J): 160- 165, I WW. O 1999 I. ippincotl Williams & Wilkins, Inc., Philadelphia Bedside Tests of Saccades After Head Injury Lindsay E. Mulhall, Dip. App. So. ( Orth), Isla M. Williams, M. D. F. R. A. C. P., and Larry A. Abel, Ph. D. Objectives: To compare the techniques of bedside and infrared oculography tests of saccades and to compare the results of both tests in control subjects and in patients with traumatic brain injuries ( TBI). Materials and Methods: The authors elicited single memory-guided saccades, antisaccades, and self- paced saccades in 19 TBI subjects and 26 age- matched control subjects at the bedside. Taped instructions were used to ensure that the timing and sequence of each stimulus ( index finger flexion) were the same in all subjects and as close as possible to those used in both the current and previous laboratory studies. Results: Self- paced saccade rate was significantly decreased in patients with TBI. The increased error rate in single memory-guided saccades and antisaccades was not statistically significant. Conclusion: The authors concluded thai the bedside saccade tests have limited value in patients with TBI because of the range of results and large overlap of the distributions of these two groups. The number of parameters that can be measured is limited. Bedside saccade tests are easier than infrared oculography tests because the target remains visible. Key Words: Antisaccades- Rye movements- Memory-guided saccades- Self- paced saccades- Traumatic brain injury. Survivors of severe nonmissile traumatic brain injury ( TBI) have widespread cerebral damage with lasting neurologic and cognitive dysfunction. Using infrared oculography ( IRO) tests, we showed that patients recovering from severe TBI have a decreased self- paced saccade rate, impaired ability to suppress inappropriate saccades in single memory- guided and anlisaccade tests, prolonged saccadic latencies, and hypometric saccades in the visually guided reflex saccade tests ( 1). All saccades ( except the fast phases of nystagmus) are triggered by structures within the cerebral hemispheres ( 2). Saccades under different behavioral circumstances are controlled by different cortical and subcortical areas ( 2). Many patients who have sustained severe TBI have Manuscript received ; accepted. Prom the Nemo- ophthalmology Laboratory ( L. L. M, I. M. W.), Mo-uash University Department of Medicine, Alfred Hospital, Melbourne, Australia, and School of Orthoptics ( L. A. A.), La Trobe University, Melbourne, Australia. Address correspondence to Lindsay Mulhall, Dip. App. Sc. ( Orlh), c/ o Dr. Isla M. Williams, 15 Collins Street. Melbourne. Vic. 3000, Australia. other injuries that will not allow recording of eye movements with IRO in the laboratory. In the current study, we recorded voluntary control of saccades at the bedside, using tape- recorded instructions that ensured that stimuli appeared with the same timing and sequence as in the laboratory IRO tests. The testing paradigms at the bedside resembled, as closely as possible, the paradigms used in the laboratory ( I). Our aims were to compare the bedside saccade testing with tests in the laboratory using IRO and to compare their results. METHODS Subjects Patients participating in the current study had sustained a severe nonmissile traumatic brain injury and had been admitted to Bethesda Hospital, Melbourne, for rehabilitation. We excluded subjects with clinically detected impairment of vision that would affect their ability to do the tests. No patients had a visual field defect that would affect their ability to fixate on targets presented and none had neglect. We excluded subjects with clinically apparent nystagmus or third- or sixth- nerve palsies. Also excluded were patients with a history of neurologic or psychiatric disturbance and those who could not satisfactorily perform the simple visually guided saccade tests. Three of the patients were taking carbamazepinc prophylactically. Our previous study of saccades in patients with head injuries showed that carbamazepinc did not significantly influence our results ( 1). All patients included in the study had been injured in motor vehicle accidents, and most had multiple injuries that prevented their attendance at the laboratory for testing. The 19 patients aged 18 to 40 years ( mean, 24.6 years, SD, 4.9) were examined within 5 months of the head injury. All had had posttraumatic amnesia ( PTA) for more than 7 days ( range, 8- 70 days; mean, 32.1, SD, 20.3), and were therefore classified as having very severe head injuries according to Russell and Smith ( 3). All patients had emerged from PTA at least 7 days before testing. Posttraumatic amnesia duration was determined using the Westmead PTA scale ( 4). Clinical details and the results of computed tomography imaging are summarized in Table 1. Five patients were retested 6 months after the first examination. Twenty- six control subjects aged 19- 43 years ( mean, 28 years, SD, 7.1) were tested, 160 TABLK 1. Clinical and radiographic data for patients after traumatic nonmissile head injury Patient . ge/ sex PTA days Days post injury GCS on first admission Clinical findings at lime of testing and relevant immediate past history CT reports Drugs 14 15 16 17 18 19 26 M 70 144 2 3 4 5 23 l ; 22 M 25 l ; 18M 63 60 56 56 74 78 106 101 8 7 9 19 M 48 26 M 35 23 M 24 M II 40 M 8 80 ISM 47 73 61 9 10 1 1 12 13 22 M 22 M 24 F 24 F 31 M 23 21 21 19 16 27 47 40 49 62 14 3 1 1 7 15 24 25 M 14 58 21 M 14 63 25 M 14 110 106 7 Needed a lot of practice; R hemiparesis, bilal. fool drop corticospinal tract lesions affecting R more severely, convergence 8 cm. Alert, cooperative; R hemiparesis. Alert, cooperative; LSO palsy, frequent SWJ. Needed repeated instructions; L fool drop Alert, talkative; longstanding ET, L amblyopia. Overaction I. IO. Find horizontal jerk nystagmus on R gaze. Poor concentration, needed repeated instructions; R homonymous inferior quadrantic visual field defect, dysphasia, dyscalculia. Distractable; dysphonia, sensory impairment L median nerve distribution; mild palsies of RSO and RMR. 3 clays poslinjury R frontal/ parietal craniotomy for raised ICP. Alert, talkative; well controlled accommodative E. Alert, cooperative; L sciatic and L peroneal n lesions. Alert, cooperative; mild R VII nerve palsy, cerebellar ataxia. Alert, cooperative, needed reminders; mild R hemiparesis, mild R UMN facial palsy. Alert, cooperative, R brachial plexus lesion. Alert, cooperative; X', nystagmus on extreme R gaze, convergence 8 cm, familial idiopathic tremor. Alert, talkative; R optic nerve lesion. Alert, cooperative; anosmia. R pupil larger than L ( cause uncertain). Alert, cooperative; mild LLR palsy, dysphonia, mild bilat impairment of coordination. Alert; lesions R axillary, radial and suprascapular n. Repetitive I. brow movement on prolonged upgaze. Alert, talkative; positive Lhermitte's sign. Alert; previous CSE rhinorrhea. Unsteady broad based gait, slurred speech. Nystagmus on extreme L « aze. Multiple small petechial hems in posterior L parietal lobe and R ami I. frontal lobes. Soil tissue swelling in frontal and parietal lobes. Multiple cerebral contusions. Bilat frontal lobe contusions, greater in L; soft tissue swelling over R posterior parietal region. Prepontine hem. No abnormality delected. Initially no abnormality detected. 2 weeks postinjury hydrocephalus. 5 weeks poslinjury limited cerebral atrophy, lateral ventricle mildly enlarged, temporal horms enlarged, large cisterna magna. 16 months postinjury extensive areas of porencephaly in L parielo- lemporal cortex, mild venlriculomegaly, poor gray/ while differentiation. R intraventricular hem. Traumatic pneumocephalus, fracture of sphenoid, R cubit and frontal sinus. Hem- R frontal, and L frontal horn of lateral ventricle. Hem in L frontal and R temporal lobes and intraventricular hem. Hem- R intracerebral small L basal ganglia, posterior superior pons. R frontal contusions and intravenl hem. Hem in corpus callosum and L lateral ventricle. Intracerebral hem- bilat temp. 1. frontal. I, ext capsule. R basal ganglia. Hem spinal canal T6. Undisplaced fracture of floor of R orbit. Moderate cerebral oedema resolved 2 days postinjury. Intraventricular hem. Contusions- R frontal and L temporal lobes, fracture R zygomatic arch, R proptosis. No abnormality detected. No abnormality detected. lndomelh Elhinyloe CBZ Amoxycil Par + Cod CBZ lndomelh Par + Cod Fluclox Par + Cod Iilidron Paracet Heparin Par + Cod Par + Cod Paracet Par + Cod Lactulose Poloxal CBZ Paracet Par + Cod lndomelh Paracet Par + Cod Paracet Note: peripheral injuries other than to the nervous system have been omitted. Amoxycil, amoxycillin trihydrate; Bilal, bilateral; CBZ, carbamazepine; CSF, cerebrospinal fluid; CT, computed tomography; F, esophoria; ET, esotropia; Etidron, elidronatc disodium; Ethinyloe, ethinyloestradiol Icvonorgastral; Ext, External; Fluclox, flucloxacillin; GCS, Glasgow Coma Score; Hem, hemorrhage; ICP, intracranial pressure; lndomelh, indomcthacin; L. left; R. right; LIO. left inferior oblique; LLR, left lateral rectus; N, nerve, nerves; OKN, Optokinetic nystagmus; Par + Cod, Paracetamol + Codeine phosphate; Paracet, Paracetamol; Poloxal, Poloxalkol; P'FA, posttraumatic amnesia; RMR, right medial rectus; RSO, right superior oblique; LSO, left superior oblique; SW. I, square- wave jerks; UL, upper limb; LL, lower limb; UMN, upper motor neuron; LMN, lower motor neuron; X', exophoria at 33 cm. ./ Ni'iiin- Optillwliliot, Vol. 19, No. .1. I'JW 162 L. E. MULHALL ET AL. TABLE 2. Results of bedside eye movement tests at initial assessment of patients with head injuries and control subjects % errors Memory guided Anlisaeeades Saccades in 30 sees Self- paced Patients with head injuries n - 1 9 Mean ( SI)) 7.17( 5.45) 3.78 ( 3.84) 61.05 ( 12.66) Control subjects n = 26 Mean ( SD) 4.98( 6.71) 2.67 ( 3.96) 70.01 ( 13.88) p- value 2- lailed t lest 0.249 0.350 0.032* * p < 0.05. and 12 control subjects were reexamined approximately 6 months after their original tests. Procedure In this study, we have referred to all clinical saccade tests as bedside saccade tests. Informed consent was obtained from all subjects. Test protocols were approved by the Research and Ethics Committees of Bethesda Hospital and Monash University. Each subject was tested with the following: cover-uncover and alternate cover tests at near and distance, visual acuity at near, ocular movements, convergence, confrontation fields with a red hat pin, and pupil reactions to light. Patients were tested seated, except Patient 14, who was tested lying supine. Only Patient 8 needed spectacles for testing, because he had a well- controlled accommodative strabismus. The examiner sat or stood in front of the subject with her hands equidistant from the midline at approximately 20 degrees. She wore an earpiece and flexed the right or left index finger in response to the timed instruction from the audio tape. In the self- paced saccade test the earpiece was removed so that the subject and examiner could both hear the start and stop instructions. The timing and sequence of each test were as close as possible to those used in the IRO tests in the laboratory. The tests were always performed in the same order. /. Simple visually guided saccades. Subjects were instructed to look at the examiner's nose, then to look quickly and accurately at whichever finger flexed, then back to the examiner's nose. There were 16 finger flexions. This test was used to train the subjects and the results were not analyzed. 2. Memory- guided saccades. Subjects were instructed to look at the examiner's nose and to wait for the command " g o " before looking quickly and accurately at the finger that had flexed. The examiner varied the time arbitrarily between finger flexion and saying " g o " ( approximately 0.5- 1.5 seconds). At least 5 trials were given for practice and then 21 trials were administered over 85 seconds. The finger flexions, being timed by the audio tape, were separated by intervals varying from 2.5 to 5.0 seconds. The examiner counted the number of premature or incorrect glances. 3. Anlisaeeades. Subjects were instructed to look at the examiner's nose, then to look quickly and accurately at the index finger that did not move ( and not to look at 125- K • » 100- a « 75- sacc • S 50-, • P £ 25- Self- paced saccade rate o o 8 Q> o o o g* % o FIG 1. Scattergram showing self- paced saccade rate of 19 traumatically brain- injured subjects and 26 control subjects at initial assessment. the finger that flexed), and then look back to the nose. At least 5 trials were given for practice and 32 trials were given as the test over 105 seconds. The finger flexions, timed by the audio tape, were separated by intervals varying from 1.5 to 5.0 seconds. The examiner counted the errors. 4. Self- paced saccades. The examiner and subject both listened to the taped start and stop instructions. Subjects were instructed to look at the examiner's nose and, at the start instruction, look back and forth as rapidly and accurately as possible between the examiner's two index fingers ( held stationary in the same positions as for previous tests), and to continue until the stop instruction ( 30 seconds after the start). The examiner counted the number of relaxations. In the laboratory, five control subjects performed the bedside tests, followed immediately by the laboratory version of the tests in which light- emitting diodes replaced fingers as the target; a beep replaced the " go" instruction; and the eye movements were monitored by IRO. These tests and equipment have been described previously ( l). When the subjects were reviewed at 6 months, the examiner was unaware of these subjects' previous scores. Percentage error scores were calculated for single memory- guided and antisaccade tests ( number of errors/ number of finger flexions x 100). 30- 25- 20- O 10- 5 0- Error rate, memory- guided saccades o 0 o ft CD 0 o ° o oo o anP< » FIG. 2. Scattergram showing single memory- guided saccade percent error rate of 19 traumatically brain- injured subjects and 26 control subjects at initial assessment. ./ Ncum- Ophlhuhmil. Vat. IV, No. .1, I9W BEDSIDE TESTS OF SACCADES 163 15.0-, 12.5- 10.0- 7.5- 5.0- 2.5- Error rate, antlsaccades o o ODD O 1 € B O O oo OD O OO TABLE 4. A comparison, using paired I tests, of the results of bedside eye movement tests in patients with TBI at initial assessment and at 6 months Patients Controls FIG. 3. Scattergram showing antisaccade percent error rate of 19 traumatically brain- injured subjects and 26 control subjects at initial assessment. RESULTS The mean self- paced saccade rate was significantly lower in the patients with head injuries ( p = 0.032) ( Table 2), but the scatter plot ( Fig. I) shows that the range is similar in TBI subjects and control subjects. The TBI subjects had a slightly greater mean error rate than control subjects in both the single memory- guided saccades and antisaccades, but the difference did not reach statistical significance ( Table 2). The range was similar in both groups, but a greater proportion of control subjects made no errors ( Figs. 2 and 3). Five control subjects came to the laboratory. The self-paced saccade rate was similar using LEDs or fingers as targets. The control subjects made more errors in the laboratory tests of single memory- guided saccades and antisaccades than in tests using fingers as targets, but the difference was not significant ( paired t tests p - 0.144, p = 0.189) ( Table 3). The 1RO results of the 5 control subjects, tested in the laboratory, were not significantly different from the results of the 12 control subjects in the 1994 study ( 1) in memory- guided saccades, antisaccades, and self- paced saccades. After 6 months, we repeated the tests in 5 TBI subjects and 12 control subjects and found no significant change using paired t tests. There was a trend toward improvement in single memory- guided saccades and in antisaccades in patients with TBI ( p = 0.178, p = 0.089) ( Table 4) and in self- paced saccades in control subjects TABLE 3. A comparison, using paired t tests, of the results of eye movement tests in control subjects at the bedside and in the laboratory ( IRQ) % errors Memory guided Antisaceadcs Saccades in 30 sec Self- paced First visil ii = 5 Mean ( SD) 9.51 ( 6.72) 5.62( 4.64) 65( 15.65) 6- nionlh review n = 5 Mean ( SD) 3.80 ( 3.98) 2.5 ( 5.59) 72.4( 12.82) p- value 2- lailcd t lost 0.178 0.089 0.238 TBI, traumatic brain injury. ( p = 0.097) ( Table 5). No significant change was found in the control subjects ( Table 5). The results quoted were obtained using the t test ( for independent samples, or for paired samples as appropriate). Some of the data were skewed, so nonparametric tests were also performed, and they confirmed the quoted results. The significance was set at the 0.05 level. DISCUSSION Cerebral damage sustained by patients after severe TBI is widespread ( 5- 7). All patients included in this study had a PTA for more than 7 days ( Table 1) and therefore were judged to have sustained severe TBI ( 3). Both the current study and the 1994 study ( 1) showed that patients after TBI had a low self- paced saccade rale, but this had improved slightly at the 12- month review in the 1994 study. The IRO study ( 1) demonstrated the low self- paced saccade rate was caused by both multiple steps ( 1.493 steps, ± 21, control subjects 1.295, +/- 0.14, p = 0.01) and prolonged average fixation time between saccades ( 359.57 msec, +/- 153.53, control subjects 287.71 msec, +/- 48.35, p = 0.1 15), the latter suggesting impaired disengagement. At the bedside, prolonged average fixation time appeared to be the major factor slowing the self- paced saccade rate, but the multiple steps were not seen easily. The bedside self- paced saccade rate and the IRO self- paced saccade rate were similar, because the two stimuli were constantly present in both tests. In the self- paced saccade test, the subject fixated a target, disengaged fixation, generated a saccade to the TABLE 5. A comparison, using paired I tests, of the /•(' suits % errors Memory guided Antisaccades Saccades in 30 sees Sell- paced IRO. Bedside Controls n = 5 Mean ( SD) 4.76 ( 3.37) 1.88( 2.8) 73.4( 11.65) Infrared Controls n = 5 Mean ( SD) 12.33( 7.4) 6.67 ( 5.26) 70.6 ( 9.29) p- value 2- tailed I test 0.144 0.189 0.40 oj neasiae eye % errors Memory guided Antisaccades Saccades in 30 sec Self- paced movement tests assessment and First visit n = 12 Mean ( SD) 2.86( 4.91) 1.61 ( 2.98) 68.6( 12.31) in control suiije at 6 months 6- monlh review n = 12 Mean ( SD) 3.57 ( 3.59) 2.08 ( 2.43) 74.08( 7.91) :/. v at initial p- value 2- lailcd I test 0.710 0.665 0.097 J Neuio- Ophllutliitot, Vol. 19. No. J, IWV 164 L. E. MULHALL ET AL. other target, fixated, and disengaged fixation repeatedly for 30 seconds. The pathways following these eye movements are diverse ( 8- 12) and, in our subjects, included the striate cortex, because the subjects were fixating visible targets. The cerebral control of single memory-guided saccades and antisaccades involves widespread cortical and subcortical structures, including the frontal eye fields, dorsolateral prefrontal cortex, and substantia nigra. These mediate the maintenance of fixation and the initiation of the volitional saccades ( 2,9,13- 16). To allow comparison of the bedside saccade test with the IRO saccade test, taped instructions for the examiner were designed to reproduce, as closely as possible, the timing and sequence of stimuli in the laboratory. Taped instructions provided precise timing of the self- paced saccade test. Patients with TBI had a greater error rate than did control subjects in single memory- guided saccade and antisaccade tests. The difference was statistically significant in IRO tests ( 1) but not at the bedside. We suggest that the bedside saccade tests were easier. At the bedside, the subject suppressed an eye movement to a visible target and instead made a saccade to a still visible finger- after an auditory cue in a single memory- guided saccade or, to an opposite finger, when the other finger flexed in the antisaccade test. In the laboratory, the subject suppressed an eye movement to look at a point where he remembered the light to have flashed ( single memory- guided saccade test) or to a point in an equal and opposite direction to the light that flashed ( antisaccade test). The five control subjects also found the bedside single memory- guided test and antisaccade test easier. The error rate was greater in the laboratory than at the bedside ( Table 3). In each of the tests, the range of results was similar for patients and control subjects, but a greater proportion of control subjects had lower error rates ( Figs. 2 and 3). d i m e el al. ( 17) first described clinical antisaccade tests in the assessment of dementia. They found that the antisaccade error rates correlated strongly with the severity of dementia in Alzheimer's disease and, furthermore, patients with pseudo dementia had normal clinical antisaccade error rates. In our laboratory study of patients with TBI, we found that the impaired ability to suppress inappropriate saccades in single memory-guided tests and antisaccade tests was more sensitive in identifying impairment of goal- directed behavior than were the neuropsychologic tests ( 1). We found the self-paced saccade test results correlated with tests requiring visual scanning. Although the reduced self- paced saccade test results at the bedside were statistically significant, we do not recommend the clinical use of the test in patients with TBI, because of the broad and overlapping range of results in each group. Using the bedside saccade tests, we can measure error rate but not latency. In the previous study in 1994 ( 1), latency in memory- guided saccades and antisaccades significantly separated control subjects and patients with head injuries and showed significant improvement in TBI subjects. The simple visually guided saccades at the bedside were not analyzed, because bedside tests could not measure latency, accuracy, and number of steps per saccade, factors that significantly separated control subjects and patients with head injuries in the previous study but that did not show improvement over time in patients with TBI. The current study is a cautionary tale. At the bedside, the range of results and intersubject variability reduced the usefulness of these clinical tests in this population. Figures 2 and 3 show that the range of scores was similar for patients and control subjects, although a greater number of control subjects had no errors. Intersubject variability can be seen in Figs. 2 and 3. For example, in the memory- guided saccade test, 14 control subjects made no errors; however, 1 control subject had an error score of 24% and another had 19%. In antisaccades, 16 control subjects made no errors and 1 had an error score of 12%. The range of results with IRO in the previous study ( 1) was also large, but the overlap between patients with TBI and control subjects was less. Only five patients with head injuries returned for review at 6 months; the mean results of single memory-guided saccades and antisaccades improved ( Table 4), but because of the small numbers and intersubject variability, the improvement did not reach statistical significance. Twelve of the control subjects were reviewed at 6 months ( Table 5). The statistics indicated that the control subjects' self- paced saccade rate improved more than that of the head- injured patients, suggesting that improvement in these tasks may reflect practice effects rather than clinical recovery. We conclude that, in patients with TBI, bedside saccade tests have limited value, but the limitations might be less in another patient group with less diffuse neuropathology. 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