Treatment of Manifest Latent Nystagmus Alina A. Zubcov, M.D., Robert D. Reinecke, M.D., Irene Gottlob, M.D., Donelson R. Manley, M.D., and Joseph H. Calhoun, M.D.
Eight patients with manifest latent nystagmus, as noted by ocular movement recordings, were examined for nystagmus reduction after surgical or optical treatment. Seven of the patients had strabismus. Five patients underwent strabismus surgery, had no tropia postoperatively, and the manifest latent nystagmus converted to latent nystagmus. Four of these five patients subsequently showed improvement in binocular visual acuity. Three patients received optical treatment; one had accommodative esotropia and, with appropriate spectacle correction, the manifest latent nystagmus was converted to latent nystagmus with improved vision. In the other two patients the manifest latent nystagmus lessened after correction with appropriate spectacles; binocular visual acuity of one of these patients improved. The possibility of converting manifest latent nystagmus to latent nystagmus by strabismus surgery is a reasonable surgical goal. In patients with manifest latent nystagmus and strabismus, surgical or optical alignment of the eyes decreases the nystagmus intensity and may also improve binocular visual acuity. MANIFEST LATENT NYSTAGMUS is a congenital jerk form of nystagmus in which the fast phase
Accepted for publication May 21, 1990. From the Foerderer Eye Movement Center for Children (Drs. Zubcov, Reinecke, and Gottlob), and Pediatric Ophthalmology Service (Drs. Reinecke, Manley, and Calhoun), Wills Eye Hospital, Philadelphia, Pennsylvania; Department of Ophthalmology, Jefferson Medical College of Thomas Jefferson University, Philadelphia, Pennsylvania (Dr. Reinecke); and First University Eye Clinic, Vienna, Austria (Dr. Gottlob). This study was presented at the American Academy of Ophthalmology Annual Meeting in New Orleans, Louisiana, November 2,1989. Reprint requests to Robert D. Reinecke, M.D., Wills Eye Hospital, 9th and Walnut Sts., Philadelphia, PA 19107.
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is toward the fixating eye and the slow phase has decreasing velocity. It occurs when viewing binocularly (with both eyes open) but fixating monocularly. Latent nystagmus is identical to manifest latent nystagmus in wave form and differs only in its manifestation. True latent nystagmus occurs when covering or blurring the image in one eye; it is absent when viewing with both eyes. Latent nystagmus is always present in patients with manifest latent nystagmus. It has been shown that strabismus is necessary for manifest latent nystagmus, since patients with strabismus typically fixate monocularly while viewing with both eyes. This is presumably caused by cortical suppression.' Binocular visual acuity in patients with latent nystagmus is one to several lines better than the monocular visual acuity of either eye.! Through its characteristic wave form with minimal foveation time per cycle, manifest latent nystagmus and latent nystagmus are reported to be correlated with a poorer visual acuity than other wave forms or types of nystagmus.v' We investigated methods of reducing nystagmus and improving binocular visual acuity in patients with manifest latent nystagmus. In patients with latent nystagmus, binocular visual acuity was better when the nystagmus intensity decreased." One case with documented ocular movement recordings preoperatively and postoperatively has been reported.' The patient had heterotropia and manifest latent nystagmus that converted into latent nystagmus after successful surgical alignment of the eyes. No data on binocular postoperative visual acuity, however, were given. We treated eight patients in whom we performed ocular movement recordings. In six patients the manifest latent nystagmus converted to latent nystagmus, and two patients had reduced manifest latent nystagmus after successful strabismus surgery or optical alignment of the eyes. Six of the eight patients also demonstrated improved binocular visual acuities.
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Manifest Latent Nystagmus
Patients and Methods All of the patients had manifest latent nystagmus, reliable visual acuity measurements, and all received treatment. The criteria for entering the study were based on the patients' initial ocular movement recording done at the Foerderer Eye Movement Center for Children. The electro-oculographic criteria proposed by Dell'Osso, Schmidt, and Daroff" and Dell'Osso? were used to differentiate between manifest latent nystagmus, latent nystagmus, and infantile nystagmus wave forms. The manifest latent nystagmus and latent nystagmus were characterized by a typical wave form: a fast jerk followed by a slow phase decreasing in velocity. In contrast, the pendular wave form, a jerk wave form with increasing velocity of the slow phase, and triangular and torsional wave forms were thought to be consistent with infantile nystagmus. The presumed foveation time was measured as the period of time during which the ocular movement velocity was less than 2.5 degrees per second." Nystagmus intensity was defined as the nystagmus amplitude multiplied by its frequency. Eight patients met the criteria and were followed up for a mean of 1.75 years. Within this interval they were examined two to four times and treated by one of us. At least one complete ocular examination and ocular movement recording was done before treatment and one was done shortly after treatment. Binocular visual acuities were measured in primary position and in the preferred head position, if different. Monocular visual acuities were measured by two techniques: with full occlusion of the fellow eye and while holding a +4.00 spheric lens in front of the fellow eye. If the patient could not give subjective visual acuity responses, sweep visual-evoked cortical potentials were used to estimate visual acuity quantitatively." The visual acuity measurements were obtained between six and 16 weeks apart. No therapy for amblyopia was received by any of the patients within the intervening period. All patients' ocular movements were recorded on videotape at each visit. The amplitude of the nystagmus was estimated in percentage of the corneal diameter from the television tape recordings for gain standardization of the infants who had electro-oculograms. The accuracy of the estimate was ±0.25 mm. The ocular movement recordings were done
161
with a scleral, magnetic search coil system or electro-oculogram. The electro-oculography system used a Tracor RV-275 recorder and the method described by Reinecke, Guo, and Goldstein." The scleral search coil recording system has been described by Collewijn, van der Mark, and Iansen." The ocular movements were recorded over a period of three to five minutes in the straight-ahead position and in different fields of gaze with both eyes open and with each eye sequentially covered. As much as cooperation permitted, ocular movements elicited by near and far targets were recorded. In one patient (Case 8), a torsional coil recording was also performed. The proportion of occurrence of different nystagmus wave forms was estimated relative to the overall recording time.
Results The clinical and ocular movement data of our patients are given in the Table. Case 1 A 7-month-old boy had constant nystagmus and 50 prism diopters of esotropia. The wave form analysis by electro-oculography disclosed 70% manifest latent nystagmus wave form and 30% infantile nystagmus wave form (pendular) with 20- to 40-msec foveation time per cycle (Fig. 1). Visual acuity with both eyes open (by sweep visual-evoked potential) recorded at the age of 7 months was estimated to a Snellen equivalent of 20/50. Shortly after successful ocular muscle surgery, the Bruckner test disclosed orthophoria. On electro-oculography only the pendular wave form of infantile nystagmus was recorded when both eyes were open (Fig. 2). The frequency of the nystagmus did not change (3 Hz), whereas the foveation time per cycle increased to between 60 and 120 msec. The amplitude of the nystagmus, as measured in percentage of the cornea diameter from the television tape recordings, also was constant. With either eye covered, the latent nystagmus was obvious. Binocular visual acuity, by sweep visual-evoked potential, was estimated to a Snellen equivalent of 20/40, which showed a modest increase. Case 2 A 6-year-old boy who had nystagmus since infancy developed a left head turn over the past
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TABLE CLINICAL DATA OF EIGHT PATIENTS WITH NYSTAGMUS' POSTTREATMENT PRETREATMENT CASE NO., AGE (YRS)
DIAGNOSIS
BINOCULAR VISUAL ACUITY
TREATMENT
CLINICAL FINDINGS
BINOCULAR VISUAL ACUITY
1, 0.58
Infantile esotropia, nystagmus, myopia, anisometropia
20/50 (sweep VEP)
Bimedial rectus recession
Orthophoria, latent nystagmus
20/40 (sweep VEP)
2, 6
Infantile esotropia, right hypertropia, nystagmus, left head turn and tilt
20/40 (left head turn)
Horizontal Kestenbaum procedure
Orthophoria, latent nystagmus
20/25
3, 57
Acquired A pattern exotropia, nystagmus, oscillopsia
20/80
Bilateral superior oblique tenotomies
Orthophoria
20/30
4,6
Infantile esotropia, left dissociated vertical deviation, nystagmus, status postbimedial rectus recession
20/40 (before last surgery)
Left medial rectus recession, left superior rectus recession
Orthophoria, occasionally 12 P,D. left dissociated vertical deviation
20/30
5,12
Infantile esotropia, dissociated vertical deviation in both eyes, nystagmus, status postbimedial rectus recession
20/25 (before last surgery)
Inferior rectus resection
Orthophoria
20/25
6, 5
Accommodative esotropia (variable), nystagmus
20/70 (Allen cards)
Correction of hyperopia
Orthophoria, 5 P.O. exophoria, right head turn
20/38 (sweep VEP),20/40 (tumbling E)
7, 14
2-4 P.O. esotropia, 4 P.O. dissoelated vertical deviation in both eyes, status postbimedial rectus recession and bilateral rectus recession, myopia, nystagmus
20/60
Correction of myopia
Unchanged
20/60
8, 12
Orthophoria, myopia, torsional and horizontal nystagmus, stationary night blindness, right head tilt
20/50
Correction of myopia
Unchanged
20/30
'VEP indicates visual-evoked potential, and EOG indicates electro-oculogram. year, The patient had had ocular muscle surgery for infantile esotropia. At his preferred head position of 30 degrees to the left, binocular visual acuity was 20/40. In primary position he had approximately 64 P.O. of esotropia with
4 to 6 P.O. of right hypertropia. The electrooculography disclosed 20% of infantile nystagmus wave form (pendular) with a null point at 20 degrees right gaze and 80% of manifest latent nystagmus wave form (Fig. 3). After sue-
Manifest Latent Nystagmus
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TABLE (continued) CLINICAL DATA OF EIGHT PATIENTS WITH NYSTAGMUS'
163
ings. When covering either eye, latent nystagmus was still present (Fig. 4). Binocular visual acuity increased to 20/25. Postoperatively, the patient developed a right head tilt of 15 degrees.
OCULAR MOVEMENT RECORDINGS PRETREATMENT
30% infantile nystagmus wave form (pendular)
POSITREATMENT
Infantile nystagmus wave form (pendular)
and 70% manifest
and latent nystagmus
latent nystagmus wave form (EOG)
(EOG)
80% manifest latent nystagmus, 20% infantile nystagmus wave
Virtually no nystagmus in primary position, latent nystagmus (EOG)
form (EOG) Manifest latent nystagmus wave form (magnetic
Latent nystagmus (magnetic search eyecoil)
search eyecoil) Manifest latent nystagmus
Latent nystagmus (EOG)
Manifest latent nystagmus
Latent nystagmus (EOG)
Manifest latent nystagmus wave form and inter-
Latent nystagmus, intermittent pendular nystagmus at 8 Hz (EOG)
mittent pendular nystagmus at 8 Hz (EOG) Manifest latent nystagmus
Manifest latent nystagmus
wave form at 2.5 Hz and 1 degree (magnetic
at 1 Hz and .5 degrees (magnetic search
search eyecoil)
eyecoil)
Manifest latent nystagmus at 2.5 Hz (EOG) and torsional nystagmus (torsional coils)
Manifest latent nystagmus at 1.5 Hz (magnetic search eyecoil) and torsional nystagmus
cessful Kestenbaum-type ocular muscle surgery (bilateral horizontal recti recess-resect to reposition null point), the patient had orthophoria at distance by alternate cover test with virtually no nystagmus present in primary position either clinically or in ocular movement record-
Case 3 A 57-year-old man had an A pattern exotropia, orthophoria in upgaze, 30 P.D. of exotropia in primary position, and 50 P.D. of exotropia in downgaze. Nystagmus was present with both eyes open, and the patient complained of oscillopsia in downgaze. Binocular visual acuity was 20/80. Ocular movement recordings done with scleral search coils disclosed a manifest latent nystagmus wave form in all fields of gaze except superiorly, where no nystagmus was detected with both eyes open (Fig. 5). After bilateral superior oblique tenotomies were performed, the patient had orthophoria by cover test and displayed only latent nystagmus. Binocular visual acuity was 20/25, and oscillopsia was denied. The postoperative ocular movement recordings show no nystagmus under binocular conditions, but latent nystagmus was present when covering either eye (Fig. 6). Cases 4 and 5 Both patients were examined before they underwent previous surgical procedures and displayed manifest latent nystagmus wave forms. In Case 4, this 6-year-old patient, who had had previous surgery for infantile esotropia, had 20 P.D. of esotropia and 20 P.D. of left dissociated vertical deviation when first examined by us. After medial and superior rectus muscle recessions, the patient had orthophoria and binocular visual acuity improved one line. The other 12-year-old patient (Case 5), who also had had previous surgery for infantile esotropia and dissociated vertical deviation, had 12 P.D. of right dissociated vertical deviation and 18 P.D. of left dissociated vertical deviation at the first examination with us. After bilateral inferior rectus muscle resections, the patient had orthophoria. Binocular visual acuity remained unchanged at 20/25. Postoperatively, both patients had only latent nystagmus. Case 6 A 4-year-old girl simultaneously developed 25 P.D. of accommodative esotropia and nystagmus at 1 year of age. Monocular visual acuity was 20/70 in each eye. After correcting her hyperopia (R.E.: +4.00 + 1.00 x 90 and L.E.: +4.00 +0.50 X 88), she had orthophoria,
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only latent nystagmus, and showed improved binocular visual acuity of 20/40. She had a right head turn on initial use of spectacles that resolved in a short period of time. Case 7
A 14-year-old girl had manifest latent nystagmus. After appropriate correction (R.E.: -7.25 +3.50 x 20 and L.E.: - 2.25 + 1.25 x 145) of the undercorrected myopia (R.E.: -4.25 + 2.75 x 36 and L.E.: -4.50 +2.75 x 36), monocular visual acuity improved in the left eye from 20/200 to 20/60 and remained unchanged (20/ 60) in the right eye. The small esotropia (2 to 4 P.D.) and dissociated vertical deviation (4 P.D. in both eyes) remained unchanged. The manifest latent nystagmus, as noted by electro-oculography, decreased to 1 Hz and 0.5 degrees of amplitude without any change in binocular visual acuity. No foveation periods could be measured before or after treatment.
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The ocular movement recordings, done with torsional coils, showed a torsional nystagmus reduced upon right head tilt. In chin-up and chin-down position equally, the torsional movement decreased in reference to straightahead position. The horizontal electro-oculography disclosed manifest latent nystagmus at 2.5 Hz in primary position. The amplitude of the nystagmus was 8.3% of the cornea diameter as measured from the television tape. After appropriate correction (R.E.: -10.50 +2.00 x 20 and L.E.: -9.25 +1.50 x 115) of her undercorrected myopia (R.E.: -7.50 +1.50 X 58 and L.E.: -7.25 +1.25 x 116), visual acuity in the right eye improved to 20/80 and the nystagmus decreased to 1.5 Hz. The amplitude of the nystagmus measured in percentage of cornea diameter was 6.6%. Binocular visual acuity improved to 20/30.
Discussion
Case 8
A 12-year-old girl had nystagmus since the first day after birth. Binocular visual acuity in her preferred head position, right tilt of 10 to 15 degrees with chin up, was 20/50. Monocular visual acuity was R.E.: 20/200 and L.E.: 20/50. RIGHT EYE HORIZONTAL POSITION ; ;:I!
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eight patients (Cases 1 to 3 and 8) who were misidentified before the ocular movement recordings. Four of the eight patients showed a combination of wave forms: manifest latent nystagmus and infantile nystagmus in two patients (Cases 1 and 2), manifest latent nystagmus and high-frequency pendular nystagmus in one patient (Case 6), and manifest latent nystagmus with torsional nystagmus in one patient (Case 8). Dell'Osso, Schmidt, and Daroff" found that 54% of their 31 patients with manifest latent nystagmus demonstrated a combination of infantile nystagmus and manifest latent nystagmus wave forms. Recognition of these mixed types seems crucial in determining the optimal therapeutic approach and appropriate postoperative expectations of patients with nystagmus. Observations of conversion of manifest latent nystagmus into latent nystagmus were made in 1952 and 1962 by Healy12.13 who, by using an amblyoscope to move images onto the foveae of a patient with tropia, normal retinal correspondence, and nystagmus (clinically diagnosed manifest latent nystagmus), observed that the nystagmus stopped when alignment was achieved. Van Weerden and Houtman' reported one acquired case of strabismus with oscillopsia in a patient whose spontaneous nystagmus and oscillopsia disappeared after successful ocular muscle surgery. In an attempt to
elucidate the relationship between strabismus, manifest latent nystagmus, and latent nystagmus, Dell'Osso, Traccis, and Abel! described three patients, as documented by ocular movement recordings, who had no nystagmus during binocular viewing but latent nystagmus occurred when covering either eye. When the eyes assumed a tropic position, however, manifest latent nystagmus was present. We found that in the five patients who underwent successful strabismus surgery and in the one patient whose eyes were aligned through optical correction, manifest latent nystagmus was converted to latent nystagmus. We believe that the equal visual input on corresponding retinal loci the eyes receive when aligned is the cause of the conversion. Orthophoria by itself or a change in fusional status alone are not responsible for the conversion.' Dell'Osso. Traccis, and Abel! and van Weerden and Houtman" did not report the visual acuity of their patients when they were in the manifest latent nystagmus stage vs the latent nystagmus stage. In our study, four of five patients (Cases 1 to 4) with manifest latent nystagmus underwent successful strabismus surgery, subsequently demonstrated conversion of the manifest latent nystagmus into latent nystagmus, and showed improvement of binocular visual acuity (Figs. 1 to 6, Table). Also binocular visual acuities of two of the - __._'_!.. . ...r--
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166
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three patients who had optical treatment improved after the conversion of manifest latent nystagmus to latent nystagmus (Case 6) or after reduction of manifest latent nystagmus (Case 8). In Case 1 visual acuity was measured by sweep visual-evoked potential, with which we have had extensive experience for infants with various visual disorders. Our sweep visualevoked potential visual acuity estimates have correlated well with optotype visual acuity; thus we have confidence that the modest increase in visual acuity of this patient is real." This could be explained by the pendular nystagmus wave form with longer foveation time that replaced the manifest latent nystagmus. Case 2 had no nystagmus in primary position since the null point of the infantile nystagmus was therapeutically moved and the manifest latent nystagmus disappeared after the correction of the tropia. The Kestenbaum procedure is thought to improve patients' visual acuities." The less than one line improvement in this patient is probably because of the conversion of manifest latent nystagmus to latent nystagmus, as well as the result of a Kestenbaum procedure. Our findings are best demonstrated in Case 3. In this patient the complete disappearance of nystagmus when viewing binocularly can account for improved visual acuity. Two patients (Cases 4 and 5) entered the study after already undergoing one surgical procedure; therefore, we could not document their nystagmus before the first treatment but only between that one and subse-
'OO-Cov8l'8d
quent treatments. Both of these patients now have orthophoria, and the manifest latent nystagmus has converted to latent nystagmus. In Case 4, the patient has one Snellen line increase in binocular visual acuity (Table). This modest increase in a 6-year-old child might be the result of a learning effect rather than true visual acuity improvement. One patient (Case 6) showed improved binocular visual acuity after correction of the accommodative esotropia with spectacles. Improved visual acuity might have been caused by the conversion of manifest latent nystagmus to latent nystagmus. The correction of the hyperopic astigmatism may have contributed to the improvement of binocular visual acuity by improving the monocular visual acuity. In Case 8, monocular visual acuity improved after appropriate correction of the myopia. The manifest latent nystagmus also dampened. This suggests a close relationship between the level of visual acuity and the intensity of manifest latent nystagmus. We speculate as to whether visual acuity improvement makes the nystagmus better or vice versa. The better the monocular visual acuity of the fixing eye, the lower the manifest latent nystagmus intensity, as demonstrated in this patient. One of us (R.D.R.) has observed a conversion of manifest latent nystagmus to latent nystagmus while treating amblyopia in patients with manifest latent nystagmus. The lack of binocular improvement demonstrated in Case 7 seems to support the hypothesis that a decreasing amplitude of manifest latent nystag-
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Fig. 6 (Zubcov and associates). Case 3. Postoperative ocular movement recordings (magnetic scleral eye coil); binocular viewing, right eye covered, and left eye covered.
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Manifest Latent Nystagmus
mus will not improve visual acuity." Conversely, the improvement in binocular visual acuity with reduction of the manifest latent nystagmus in Case 8 is similar to the findings of Evans, Biglan, and Troost," who documented by simultaneous, quantitative ocular movement recordings and 16-mm movies that the latent nystagmus was least intense during the best recorded visual acuity of seven subjects. In Case 8 the patient had orthophoria and both manifest latent nystagmus and torsional nystagmus (infantile nystagmus) with a right head tilt of 10 to 15 degrees with the chin up. The early occurrence suggested infantile nystagmus. Subsequent wave form analysis, however, disclosed a typical manifest latent nystagmus, jerk nystagmus, along with an additional torsional component. This patient does not have tropia along with the manifest latent nystagmus. Lang" reported that only two of 198 patients with latent nystagmus had no strabismus. Dell'Osso, Traccis, and Abel' considered strabismus (phoria or tropia) a necessary but insufficient cause of manifest latent nystagmus or latent nystagmus. Possibly in Case 8 the patient had a small-angle tropia that was not detected because of the high-amplitude latent nystagmus. Four of our five patients who had operations for esotropia had symmetric surgery. The manifest latent nystagmus lessened whenever alignment of the eyes was achieved. Ishikawa" performed a recess-resect surgical procedure on his five esotropic patients which, he believed, gave better results with regard to the intensity of nystagmus and visual function. There are no data in his study, however, to substantiate this claim. Metz and Smith'? described one patient who underwent symmetric surgery with good postoperative results with regard to the nystagmus intensity. Whether symmetric or asymmetric surgery is the better approach in patients with manifest latent nystagmus is debatable. The improvement in visual acuity obtained in two of our eight patients (Cases 3 and 4) points to the manifest latent nystagmus conversion as a cause. In four of the patients (Cases 1, 2, 6, and 8) other plausible explanations may be the cause of our reported improvement such as newer, less proven techniques of assessing visual acuity, simultaneous surgical procedures, optical corrections, or learning effects. Ocular muscle surgery in patients with manifest latent nystagmus seems to have not only a cosmetic effect, but it also converts manifest latent nystagmus into latent nystagmus.
References 1. Dell'Osso, L. F., Traccis, S., and Abel, 1. A.: Strabismus. A necessary condition for latent and manifest latent nystagmus. Neuro-ophthalmology 3:247,1983. 2. Evans, D. E., Biglan, A. W., and Troost, B. T.: Measurement of visual acuity in latent nystagmus. Ophthalmology 88:134,1981. 3. Dell'Osso, L. F., Ellenberger, c.. [r., Abel, L. A., and Flynn, J. T.: The nystagmus blockage syndrome. Invest. Ophthalmol. Vis. Sci. 24:1580, 1983. 4. Reinecke, R. D., and Zubcov, A. A.: Treatable nystagmus. Proceedings of the Sixth Meeting of the International Strabismological Association, Brisbane, Australia, March 11-16, 1990. In press. 5. van Weerden, T. W., and Houtman, W. A.: Manifest latent nystagmus of late onset. A case report. Ophthalmologica 188:153, 1984. 6. Dell'Osso, L. F., Schmidt, D., and Daroff, R. B.: Latent, manifest latent, and congenital nystagmus. Arch. Ophthalmol. 97:1877, 1979. 7. Dell'Osso, 1. F.: Congenital, latent and manifest latent nystagmus. Similarities, differences and relations to strabismus. [pn. J. Ophthalmol. 29:351, 1985. 8. Dickinson, C. M., and Abadi, R. V.: The influence of nystagmoid oscillation on contrast sensitivity in normal observer. Vision Res. 25:1089, 1985. 9. Gottlob, I., Fendick, M. G., Guo, S., Zubcov, A. A., Odom, J. V., and Reinecke, R. D.: Visual acuity measurements by swept spatial frequency visualevoked-cortical potentials (VECPs). Clinical application in children with various visual disorders. J. Pediatr. Ophthalmol. Strabismus 27:40, 1990. 10. Reinecke, R. D., Guo, S., and Goldstein, H. P.: Wave form evolution in infantile nystagmus. An electro-oculographic study of 35 cases. Binoc. Vis. 3: 191, 1988. 11. Collewijn, H., van der Mark, F., and Jansen, T. c.: Precise recording of human eye movements. Vision Res. 15:447, 1975. 12. Healy, E.: Nystagmus treated by orthoptics. Am. Orthopt. J. 2:53, 1952. 13. - - : Nystagmus treated by orthoptics. A second report. Am. Orthopt. J. 12:89, 1962. 14. Kaufmann, H., and Kolling, G.: Operative Therapie bei nystagmuspatienten mit binocularfunktionen mit und ohne Kopfzwangshaltung. Ber. Dtsch. Ophthalmol. Ges. 78:815, 1981. 15. Lang, J.: Nystagmus probleme in der praxis. Klin. Monatsbl. Augenheilkd. 172:410, 1978. 16. Ishikawa, S.: Latent nystagmus and its etiology. In Reinecke, R. D. (ed.): Strabismus II. Proceedings of the Third Meeting of the International Strabismological Association. New York, Grune and Stratton, 1979, pp. 203-214. 17. Metz, H. S., and Smith, G.: Abduction nystagmus. J. Pediatr. Ophthalmol. Strabismus 15:312, 1978.
Eight patients with manifest latent nystagmus, as noted by ocular movement recordings, were examined for nystagmus reduction after surgical or optical treatment. Seven of the patients had strabismus. Five patients underwent strabismus surgery, had no tropia postoperatively, and the manifest latent nystagmus converted to latent nystagmus. Four of these five patients subsequently showed improvement in binocular visual acuity. Three patients received optical treatment; one had accommodative esotropia and, with appropriate spectacle correction, the manifest latent nystagmus was converted to latent nystagmus with improved vision. In the other two patients the manifest latent nystagmus lessened after correction with appropriate spectacles; binocular visual acuity of one of these patients improved. The possibility of converting manifest latent nystagmus to latent nystagmus by strabismus surgery is a reasonable surgical goal. In patients with manifest latent nystagmus and strabismus, surgical or optical alignment of the eyes decreases the nystagmus intensity and may also improve binocular visual acuity. MANIFEST LATENT NYSTAGMUS is a congenital jerk form of nystagmus in which the fast phase
Accepted for publication May 21, 1990. From the Foerderer Eye Movement Center for Children (Drs. Zubcov, Reinecke, and Gottlob), and Pediatric Ophthalmology Service (Drs. Reinecke, Manley, and Calhoun), Wills Eye Hospital, Philadelphia, Pennsylvania; Department of Ophthalmology, Jefferson Medical College of Thomas Jefferson University, Philadelphia, Pennsylvania (Dr. Reinecke); and First University Eye Clinic, Vienna, Austria (Dr. Gottlob). This study was presented at the American Academy of Ophthalmology Annual Meeting in New Orleans, Louisiana, November 2,1989. Reprint requests to Robert D. Reinecke, M.D., Wills Eye Hospital, 9th and Walnut Sts., Philadelphia, PA 19107.
160
is toward the fixating eye and the slow phase has decreasing velocity. It occurs when viewing binocularly (with both eyes open) but fixating monocularly. Latent nystagmus is identical to manifest latent nystagmus in wave form and differs only in its manifestation. True latent nystagmus occurs when covering or blurring the image in one eye; it is absent when viewing with both eyes. Latent nystagmus is always present in patients with manifest latent nystagmus. It has been shown that strabismus is necessary for manifest latent nystagmus, since patients with strabismus typically fixate monocularly while viewing with both eyes. This is presumably caused by cortical suppression.' Binocular visual acuity in patients with latent nystagmus is one to several lines better than the monocular visual acuity of either eye.! Through its characteristic wave form with minimal foveation time per cycle, manifest latent nystagmus and latent nystagmus are reported to be correlated with a poorer visual acuity than other wave forms or types of nystagmus.v' We investigated methods of reducing nystagmus and improving binocular visual acuity in patients with manifest latent nystagmus. In patients with latent nystagmus, binocular visual acuity was better when the nystagmus intensity decreased." One case with documented ocular movement recordings preoperatively and postoperatively has been reported.' The patient had heterotropia and manifest latent nystagmus that converted into latent nystagmus after successful surgical alignment of the eyes. No data on binocular postoperative visual acuity, however, were given. We treated eight patients in whom we performed ocular movement recordings. In six patients the manifest latent nystagmus converted to latent nystagmus, and two patients had reduced manifest latent nystagmus after successful strabismus surgery or optical alignment of the eyes. Six of the eight patients also demonstrated improved binocular visual acuities.
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Manifest Latent Nystagmus
Patients and Methods All of the patients had manifest latent nystagmus, reliable visual acuity measurements, and all received treatment. The criteria for entering the study were based on the patients' initial ocular movement recording done at the Foerderer Eye Movement Center for Children. The electro-oculographic criteria proposed by Dell'Osso, Schmidt, and Daroff" and Dell'Osso? were used to differentiate between manifest latent nystagmus, latent nystagmus, and infantile nystagmus wave forms. The manifest latent nystagmus and latent nystagmus were characterized by a typical wave form: a fast jerk followed by a slow phase decreasing in velocity. In contrast, the pendular wave form, a jerk wave form with increasing velocity of the slow phase, and triangular and torsional wave forms were thought to be consistent with infantile nystagmus. The presumed foveation time was measured as the period of time during which the ocular movement velocity was less than 2.5 degrees per second." Nystagmus intensity was defined as the nystagmus amplitude multiplied by its frequency. Eight patients met the criteria and were followed up for a mean of 1.75 years. Within this interval they were examined two to four times and treated by one of us. At least one complete ocular examination and ocular movement recording was done before treatment and one was done shortly after treatment. Binocular visual acuities were measured in primary position and in the preferred head position, if different. Monocular visual acuities were measured by two techniques: with full occlusion of the fellow eye and while holding a +4.00 spheric lens in front of the fellow eye. If the patient could not give subjective visual acuity responses, sweep visual-evoked cortical potentials were used to estimate visual acuity quantitatively." The visual acuity measurements were obtained between six and 16 weeks apart. No therapy for amblyopia was received by any of the patients within the intervening period. All patients' ocular movements were recorded on videotape at each visit. The amplitude of the nystagmus was estimated in percentage of the corneal diameter from the television tape recordings for gain standardization of the infants who had electro-oculograms. The accuracy of the estimate was ±0.25 mm. The ocular movement recordings were done
161
with a scleral, magnetic search coil system or electro-oculogram. The electro-oculography system used a Tracor RV-275 recorder and the method described by Reinecke, Guo, and Goldstein." The scleral search coil recording system has been described by Collewijn, van der Mark, and Iansen." The ocular movements were recorded over a period of three to five minutes in the straight-ahead position and in different fields of gaze with both eyes open and with each eye sequentially covered. As much as cooperation permitted, ocular movements elicited by near and far targets were recorded. In one patient (Case 8), a torsional coil recording was also performed. The proportion of occurrence of different nystagmus wave forms was estimated relative to the overall recording time.
Results The clinical and ocular movement data of our patients are given in the Table. Case 1 A 7-month-old boy had constant nystagmus and 50 prism diopters of esotropia. The wave form analysis by electro-oculography disclosed 70% manifest latent nystagmus wave form and 30% infantile nystagmus wave form (pendular) with 20- to 40-msec foveation time per cycle (Fig. 1). Visual acuity with both eyes open (by sweep visual-evoked potential) recorded at the age of 7 months was estimated to a Snellen equivalent of 20/50. Shortly after successful ocular muscle surgery, the Bruckner test disclosed orthophoria. On electro-oculography only the pendular wave form of infantile nystagmus was recorded when both eyes were open (Fig. 2). The frequency of the nystagmus did not change (3 Hz), whereas the foveation time per cycle increased to between 60 and 120 msec. The amplitude of the nystagmus, as measured in percentage of the cornea diameter from the television tape recordings, also was constant. With either eye covered, the latent nystagmus was obvious. Binocular visual acuity, by sweep visual-evoked potential, was estimated to a Snellen equivalent of 20/40, which showed a modest increase. Case 2 A 6-year-old boy who had nystagmus since infancy developed a left head turn over the past
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TABLE CLINICAL DATA OF EIGHT PATIENTS WITH NYSTAGMUS' POSTTREATMENT PRETREATMENT CASE NO., AGE (YRS)
DIAGNOSIS
BINOCULAR VISUAL ACUITY
TREATMENT
CLINICAL FINDINGS
BINOCULAR VISUAL ACUITY
1, 0.58
Infantile esotropia, nystagmus, myopia, anisometropia
20/50 (sweep VEP)
Bimedial rectus recession
Orthophoria, latent nystagmus
20/40 (sweep VEP)
2, 6
Infantile esotropia, right hypertropia, nystagmus, left head turn and tilt
20/40 (left head turn)
Horizontal Kestenbaum procedure
Orthophoria, latent nystagmus
20/25
3, 57
Acquired A pattern exotropia, nystagmus, oscillopsia
20/80
Bilateral superior oblique tenotomies
Orthophoria
20/30
4,6
Infantile esotropia, left dissociated vertical deviation, nystagmus, status postbimedial rectus recession
20/40 (before last surgery)
Left medial rectus recession, left superior rectus recession
Orthophoria, occasionally 12 P,D. left dissociated vertical deviation
20/30
5,12
Infantile esotropia, dissociated vertical deviation in both eyes, nystagmus, status postbimedial rectus recession
20/25 (before last surgery)
Inferior rectus resection
Orthophoria
20/25
6, 5
Accommodative esotropia (variable), nystagmus
20/70 (Allen cards)
Correction of hyperopia
Orthophoria, 5 P.O. exophoria, right head turn
20/38 (sweep VEP),20/40 (tumbling E)
7, 14
2-4 P.O. esotropia, 4 P.O. dissoelated vertical deviation in both eyes, status postbimedial rectus recession and bilateral rectus recession, myopia, nystagmus
20/60
Correction of myopia
Unchanged
20/60
8, 12
Orthophoria, myopia, torsional and horizontal nystagmus, stationary night blindness, right head tilt
20/50
Correction of myopia
Unchanged
20/30
'VEP indicates visual-evoked potential, and EOG indicates electro-oculogram. year, The patient had had ocular muscle surgery for infantile esotropia. At his preferred head position of 30 degrees to the left, binocular visual acuity was 20/40. In primary position he had approximately 64 P.O. of esotropia with
4 to 6 P.O. of right hypertropia. The electrooculography disclosed 20% of infantile nystagmus wave form (pendular) with a null point at 20 degrees right gaze and 80% of manifest latent nystagmus wave form (Fig. 3). After sue-
Manifest Latent Nystagmus
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TABLE (continued) CLINICAL DATA OF EIGHT PATIENTS WITH NYSTAGMUS'
163
ings. When covering either eye, latent nystagmus was still present (Fig. 4). Binocular visual acuity increased to 20/25. Postoperatively, the patient developed a right head tilt of 15 degrees.
OCULAR MOVEMENT RECORDINGS PRETREATMENT
30% infantile nystagmus wave form (pendular)
POSITREATMENT
Infantile nystagmus wave form (pendular)
and 70% manifest
and latent nystagmus
latent nystagmus wave form (EOG)
(EOG)
80% manifest latent nystagmus, 20% infantile nystagmus wave
Virtually no nystagmus in primary position, latent nystagmus (EOG)
form (EOG) Manifest latent nystagmus wave form (magnetic
Latent nystagmus (magnetic search eyecoil)
search eyecoil) Manifest latent nystagmus
Latent nystagmus (EOG)
Manifest latent nystagmus
Latent nystagmus (EOG)
Manifest latent nystagmus wave form and inter-
Latent nystagmus, intermittent pendular nystagmus at 8 Hz (EOG)
mittent pendular nystagmus at 8 Hz (EOG) Manifest latent nystagmus
Manifest latent nystagmus
wave form at 2.5 Hz and 1 degree (magnetic
at 1 Hz and .5 degrees (magnetic search
search eyecoil)
eyecoil)
Manifest latent nystagmus at 2.5 Hz (EOG) and torsional nystagmus (torsional coils)
Manifest latent nystagmus at 1.5 Hz (magnetic search eyecoil) and torsional nystagmus
cessful Kestenbaum-type ocular muscle surgery (bilateral horizontal recti recess-resect to reposition null point), the patient had orthophoria at distance by alternate cover test with virtually no nystagmus present in primary position either clinically or in ocular movement record-
Case 3 A 57-year-old man had an A pattern exotropia, orthophoria in upgaze, 30 P.D. of exotropia in primary position, and 50 P.D. of exotropia in downgaze. Nystagmus was present with both eyes open, and the patient complained of oscillopsia in downgaze. Binocular visual acuity was 20/80. Ocular movement recordings done with scleral search coils disclosed a manifest latent nystagmus wave form in all fields of gaze except superiorly, where no nystagmus was detected with both eyes open (Fig. 5). After bilateral superior oblique tenotomies were performed, the patient had orthophoria by cover test and displayed only latent nystagmus. Binocular visual acuity was 20/25, and oscillopsia was denied. The postoperative ocular movement recordings show no nystagmus under binocular conditions, but latent nystagmus was present when covering either eye (Fig. 6). Cases 4 and 5 Both patients were examined before they underwent previous surgical procedures and displayed manifest latent nystagmus wave forms. In Case 4, this 6-year-old patient, who had had previous surgery for infantile esotropia, had 20 P.D. of esotropia and 20 P.D. of left dissociated vertical deviation when first examined by us. After medial and superior rectus muscle recessions, the patient had orthophoria and binocular visual acuity improved one line. The other 12-year-old patient (Case 5), who also had had previous surgery for infantile esotropia and dissociated vertical deviation, had 12 P.D. of right dissociated vertical deviation and 18 P.D. of left dissociated vertical deviation at the first examination with us. After bilateral inferior rectus muscle resections, the patient had orthophoria. Binocular visual acuity remained unchanged at 20/25. Postoperatively, both patients had only latent nystagmus. Case 6 A 4-year-old girl simultaneously developed 25 P.D. of accommodative esotropia and nystagmus at 1 year of age. Monocular visual acuity was 20/70 in each eye. After correcting her hyperopia (R.E.: +4.00 + 1.00 x 90 and L.E.: +4.00 +0.50 X 88), she had orthophoria,
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only latent nystagmus, and showed improved binocular visual acuity of 20/40. She had a right head turn on initial use of spectacles that resolved in a short period of time. Case 7
A 14-year-old girl had manifest latent nystagmus. After appropriate correction (R.E.: -7.25 +3.50 x 20 and L.E.: - 2.25 + 1.25 x 145) of the undercorrected myopia (R.E.: -4.25 + 2.75 x 36 and L.E.: -4.50 +2.75 x 36), monocular visual acuity improved in the left eye from 20/200 to 20/60 and remained unchanged (20/ 60) in the right eye. The small esotropia (2 to 4 P.D.) and dissociated vertical deviation (4 P.D. in both eyes) remained unchanged. The manifest latent nystagmus, as noted by electro-oculography, decreased to 1 Hz and 0.5 degrees of amplitude without any change in binocular visual acuity. No foveation periods could be measured before or after treatment.
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The ocular movement recordings, done with torsional coils, showed a torsional nystagmus reduced upon right head tilt. In chin-up and chin-down position equally, the torsional movement decreased in reference to straightahead position. The horizontal electro-oculography disclosed manifest latent nystagmus at 2.5 Hz in primary position. The amplitude of the nystagmus was 8.3% of the cornea diameter as measured from the television tape. After appropriate correction (R.E.: -10.50 +2.00 x 20 and L.E.: -9.25 +1.50 x 115) of her undercorrected myopia (R.E.: -7.50 +1.50 X 58 and L.E.: -7.25 +1.25 x 116), visual acuity in the right eye improved to 20/80 and the nystagmus decreased to 1.5 Hz. The amplitude of the nystagmus measured in percentage of cornea diameter was 6.6%. Binocular visual acuity improved to 20/30.
Discussion
Case 8
A 12-year-old girl had nystagmus since the first day after birth. Binocular visual acuity in her preferred head position, right tilt of 10 to 15 degrees with chin up, was 20/50. Monocular visual acuity was R.E.: 20/200 and L.E.: 20/50. RIGHT EYE HORIZONTAL POSITION ; ;:I!
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eight patients (Cases 1 to 3 and 8) who were misidentified before the ocular movement recordings. Four of the eight patients showed a combination of wave forms: manifest latent nystagmus and infantile nystagmus in two patients (Cases 1 and 2), manifest latent nystagmus and high-frequency pendular nystagmus in one patient (Case 6), and manifest latent nystagmus with torsional nystagmus in one patient (Case 8). Dell'Osso, Schmidt, and Daroff" found that 54% of their 31 patients with manifest latent nystagmus demonstrated a combination of infantile nystagmus and manifest latent nystagmus wave forms. Recognition of these mixed types seems crucial in determining the optimal therapeutic approach and appropriate postoperative expectations of patients with nystagmus. Observations of conversion of manifest latent nystagmus into latent nystagmus were made in 1952 and 1962 by Healy12.13 who, by using an amblyoscope to move images onto the foveae of a patient with tropia, normal retinal correspondence, and nystagmus (clinically diagnosed manifest latent nystagmus), observed that the nystagmus stopped when alignment was achieved. Van Weerden and Houtman' reported one acquired case of strabismus with oscillopsia in a patient whose spontaneous nystagmus and oscillopsia disappeared after successful ocular muscle surgery. In an attempt to
elucidate the relationship between strabismus, manifest latent nystagmus, and latent nystagmus, Dell'Osso, Traccis, and Abel! described three patients, as documented by ocular movement recordings, who had no nystagmus during binocular viewing but latent nystagmus occurred when covering either eye. When the eyes assumed a tropic position, however, manifest latent nystagmus was present. We found that in the five patients who underwent successful strabismus surgery and in the one patient whose eyes were aligned through optical correction, manifest latent nystagmus was converted to latent nystagmus. We believe that the equal visual input on corresponding retinal loci the eyes receive when aligned is the cause of the conversion. Orthophoria by itself or a change in fusional status alone are not responsible for the conversion.' Dell'Osso. Traccis, and Abel! and van Weerden and Houtman" did not report the visual acuity of their patients when they were in the manifest latent nystagmus stage vs the latent nystagmus stage. In our study, four of five patients (Cases 1 to 4) with manifest latent nystagmus underwent successful strabismus surgery, subsequently demonstrated conversion of the manifest latent nystagmus into latent nystagmus, and showed improvement of binocular visual acuity (Figs. 1 to 6, Table). Also binocular visual acuities of two of the - __._'_!.. . ...r--
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166
AMERICAN JOURNAL OF OPHTHALMOLOGY
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three patients who had optical treatment improved after the conversion of manifest latent nystagmus to latent nystagmus (Case 6) or after reduction of manifest latent nystagmus (Case 8). In Case 1 visual acuity was measured by sweep visual-evoked potential, with which we have had extensive experience for infants with various visual disorders. Our sweep visualevoked potential visual acuity estimates have correlated well with optotype visual acuity; thus we have confidence that the modest increase in visual acuity of this patient is real." This could be explained by the pendular nystagmus wave form with longer foveation time that replaced the manifest latent nystagmus. Case 2 had no nystagmus in primary position since the null point of the infantile nystagmus was therapeutically moved and the manifest latent nystagmus disappeared after the correction of the tropia. The Kestenbaum procedure is thought to improve patients' visual acuities." The less than one line improvement in this patient is probably because of the conversion of manifest latent nystagmus to latent nystagmus, as well as the result of a Kestenbaum procedure. Our findings are best demonstrated in Case 3. In this patient the complete disappearance of nystagmus when viewing binocularly can account for improved visual acuity. Two patients (Cases 4 and 5) entered the study after already undergoing one surgical procedure; therefore, we could not document their nystagmus before the first treatment but only between that one and subse-
'OO-Cov8l'8d
quent treatments. Both of these patients now have orthophoria, and the manifest latent nystagmus has converted to latent nystagmus. In Case 4, the patient has one Snellen line increase in binocular visual acuity (Table). This modest increase in a 6-year-old child might be the result of a learning effect rather than true visual acuity improvement. One patient (Case 6) showed improved binocular visual acuity after correction of the accommodative esotropia with spectacles. Improved visual acuity might have been caused by the conversion of manifest latent nystagmus to latent nystagmus. The correction of the hyperopic astigmatism may have contributed to the improvement of binocular visual acuity by improving the monocular visual acuity. In Case 8, monocular visual acuity improved after appropriate correction of the myopia. The manifest latent nystagmus also dampened. This suggests a close relationship between the level of visual acuity and the intensity of manifest latent nystagmus. We speculate as to whether visual acuity improvement makes the nystagmus better or vice versa. The better the monocular visual acuity of the fixing eye, the lower the manifest latent nystagmus intensity, as demonstrated in this patient. One of us (R.D.R.) has observed a conversion of manifest latent nystagmus to latent nystagmus while treating amblyopia in patients with manifest latent nystagmus. The lack of binocular improvement demonstrated in Case 7 seems to support the hypothesis that a decreasing amplitude of manifest latent nystag-
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Fig. 6 (Zubcov and associates). Case 3. Postoperative ocular movement recordings (magnetic scleral eye coil); binocular viewing, right eye covered, and left eye covered.
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Manifest Latent Nystagmus
mus will not improve visual acuity." Conversely, the improvement in binocular visual acuity with reduction of the manifest latent nystagmus in Case 8 is similar to the findings of Evans, Biglan, and Troost," who documented by simultaneous, quantitative ocular movement recordings and 16-mm movies that the latent nystagmus was least intense during the best recorded visual acuity of seven subjects. In Case 8 the patient had orthophoria and both manifest latent nystagmus and torsional nystagmus (infantile nystagmus) with a right head tilt of 10 to 15 degrees with the chin up. The early occurrence suggested infantile nystagmus. Subsequent wave form analysis, however, disclosed a typical manifest latent nystagmus, jerk nystagmus, along with an additional torsional component. This patient does not have tropia along with the manifest latent nystagmus. Lang" reported that only two of 198 patients with latent nystagmus had no strabismus. Dell'Osso, Traccis, and Abel' considered strabismus (phoria or tropia) a necessary but insufficient cause of manifest latent nystagmus or latent nystagmus. Possibly in Case 8 the patient had a small-angle tropia that was not detected because of the high-amplitude latent nystagmus. Four of our five patients who had operations for esotropia had symmetric surgery. The manifest latent nystagmus lessened whenever alignment of the eyes was achieved. Ishikawa" performed a recess-resect surgical procedure on his five esotropic patients which, he believed, gave better results with regard to the intensity of nystagmus and visual function. There are no data in his study, however, to substantiate this claim. Metz and Smith'? described one patient who underwent symmetric surgery with good postoperative results with regard to the nystagmus intensity. Whether symmetric or asymmetric surgery is the better approach in patients with manifest latent nystagmus is debatable. The improvement in visual acuity obtained in two of our eight patients (Cases 3 and 4) points to the manifest latent nystagmus conversion as a cause. In four of the patients (Cases 1, 2, 6, and 8) other plausible explanations may be the cause of our reported improvement such as newer, less proven techniques of assessing visual acuity, simultaneous surgical procedures, optical corrections, or learning effects. Ocular muscle surgery in patients with manifest latent nystagmus seems to have not only a cosmetic effect, but it also converts manifest latent nystagmus into latent nystagmus.
References 1. Dell'Osso, L. F., Traccis, S., and Abel, 1. A.: Strabismus. A necessary condition for latent and manifest latent nystagmus. Neuro-ophthalmology 3:247,1983. 2. Evans, D. E., Biglan, A. W., and Troost, B. T.: Measurement of visual acuity in latent nystagmus. Ophthalmology 88:134,1981. 3. Dell'Osso, L. F., Ellenberger, c.. [r., Abel, L. A., and Flynn, J. T.: The nystagmus blockage syndrome. Invest. Ophthalmol. Vis. Sci. 24:1580, 1983. 4. Reinecke, R. D., and Zubcov, A. A.: Treatable nystagmus. Proceedings of the Sixth Meeting of the International Strabismological Association, Brisbane, Australia, March 11-16, 1990. In press. 5. van Weerden, T. W., and Houtman, W. A.: Manifest latent nystagmus of late onset. A case report. Ophthalmologica 188:153, 1984. 6. Dell'Osso, L. F., Schmidt, D., and Daroff, R. B.: Latent, manifest latent, and congenital nystagmus. Arch. Ophthalmol. 97:1877, 1979. 7. Dell'Osso, 1. F.: Congenital, latent and manifest latent nystagmus. Similarities, differences and relations to strabismus. [pn. J. Ophthalmol. 29:351, 1985. 8. Dickinson, C. M., and Abadi, R. V.: The influence of nystagmoid oscillation on contrast sensitivity in normal observer. Vision Res. 25:1089, 1985. 9. Gottlob, I., Fendick, M. G., Guo, S., Zubcov, A. A., Odom, J. V., and Reinecke, R. D.: Visual acuity measurements by swept spatial frequency visualevoked-cortical potentials (VECPs). Clinical application in children with various visual disorders. J. Pediatr. Ophthalmol. Strabismus 27:40, 1990. 10. Reinecke, R. D., Guo, S., and Goldstein, H. P.: Wave form evolution in infantile nystagmus. An electro-oculographic study of 35 cases. Binoc. Vis. 3: 191, 1988. 11. Collewijn, H., van der Mark, F., and Jansen, T. c.: Precise recording of human eye movements. Vision Res. 15:447, 1975. 12. Healy, E.: Nystagmus treated by orthoptics. Am. Orthopt. J. 2:53, 1952. 13. - - : Nystagmus treated by orthoptics. A second report. Am. Orthopt. J. 12:89, 1962. 14. Kaufmann, H., and Kolling, G.: Operative Therapie bei nystagmuspatienten mit binocularfunktionen mit und ohne Kopfzwangshaltung. Ber. Dtsch. Ophthalmol. Ges. 78:815, 1981. 15. Lang, J.: Nystagmus probleme in der praxis. Klin. Monatsbl. Augenheilkd. 172:410, 1978. 16. Ishikawa, S.: Latent nystagmus and its etiology. In Reinecke, R. D. (ed.): Strabismus II. Proceedings of the Third Meeting of the International Strabismological Association. New York, Grune and Stratton, 1979, pp. 203-214. 17. Metz, H. S., and Smith, G.: Abduction nystagmus. J. Pediatr. Ophthalmol. Strabismus 15:312, 1978.
