Strabismus, 2014; 22(2): 81–85 ! Informa Healthcare USA, Inc. ISSN: 0927-3972 print / 1744-5132 online DOI: 10.3109/09273972.2014.904898
Long-term results of four horizontal rectus muscle recession in nystagmus treatment Huban Atilla,
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1
1
MD
, Helin Deniz Demir,
MD
2
, and Yusuf I¸s ıkc¸elik,
MD
3
Faculty of Medicine, Department of Ophthalmology, Ankara University, Ankara, Turkey, 2Faculty of Medicine, Department of Ophthalmology, Tokat Gaziosmanpa¸sa University, Tokat, Turkey, and 3U¸sak Eye Center, U¸sak, Turkey
ABSTRACT Purpose: To report the long-term results of four horizontal rectus muscle recessions that were performed for infantile nystagmus syndrome treatment. Methods: In this case series, patients with infantile nystagmus syndrome who had four horizontal muscle recessions previously were recruited and ophthalmological examination and electronystagmography recordings were performed. Objectively, amplitude and frequency of nystagmus were measured from the recordings and the intensity was calculated. Visual acuity, stereopsis, and alignment were evaluated and compared with the preoperative and postoperative values. Results: The records of the 12 patients who had four horizontal rectus muscle recession surgery were evaluated and six patients (5 male, 1 female) who had regular follow-ups were included in this study. Mean follow-up was 14.17 ± 0.41 years (minimum 14 years, maximum 15 years) and mean age of patients at the last visit was 22 years (20-28 years). On subjective evaluation, two-thirds (4/6) of the patients were satisfied with the surgical results and had the impression that after surgery, nystagmus decreased in intensity and head posture improved. On objective evaluation, visual acuity was found to be the same, however, stereopsis improved (preoperatively and postoperatively median stereopsis was 600 sec arc vs 200 sec arc final). The decrease in nystagmus amplitude and frequency was still maintained. Conclusions: Nystagmus surgery on four horizontal rectus muscles has positive effects on binocular function and nystagmus parameters in the long-term follow-up. As we could not treat the primary pathology, the visual acuity was about the same but the decrease in nystagmus amplitude and frequency was still maintained with better stereopsis, and patient satisfaction. Keywords: Electronystagmography, infantile nystagmus syndrome, nystagmus, nystagmus surgery
INTRODUCTION
treatment modality for INS due to associated visual sensory system abnormalities or inherited underlying defects. Therefore the main goal of the treatment for nystagmus is usually to reduce the intensity of the nystagmus in order to increase foveation time or to shift the gaze position with the lowest nystagmus frequency (null zone) to the primary position and to decrease or eliminate head posture. There are different surgical treatment modalities that are widely known such as Anderson-Kestenbaum, Anderson, four horizontal rectus muscle recession, or tenotomy
Infantile nystagmus syndrome (INS) is an ocularmotor disorder of unknown etiology that presents at birth or early infancy and is clinically characterized by involuntary oscillations of the eyes.1,2 Estimations of the incidence of INS vary from 0.03% to 0.0005%; the generally accepted figure is 0.015%. Patients with INS usually have diminished visual acuity and this may be inversely related to the intensity of the nystagmus.1 Unfortunately there is no radical or highly effective
Received 23 May 2013; Revised 13 November 2013; Accepted 5 February 2014; Published online 28 April 2014 Correspondence: Prof Dr Huban Atilla, Faculty of Medicine, Department of Ophthalmology, Ankara University, Mamak cad no: 4 Dikimevi _ ¨ RKIYE. Ankara, 06260 TU Tel: 90 532 4541604. Fax: 90 312 466 66 31. E-mail: [email protected]
81
82 H. Atilla et al. of the recti, however long-term effects are not definitely described. The aim of this study is to report the long-term results of four muscle recession in infantile nystagmus syndrome patients.
TABLE 1. The gender and diagnosis of the patients and their ages at the time of operation and at the time of last visit (M: male, F: female). Patient # (sex)
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MATERIALS AND METHODS The results of the initial study were published previously.3 The records of the 12 patients who had nystagmus surgery were evaluated and 6 patients (5 male, 1 female) who had regular follow-ups were included in the current study. All procedures followed the declaration of Helsinki and informed consent forms were filled out and signed by the parents or patients. For inclusion in the study, the patients who had a follow-up period of at least 10 years were included. All of the patients in the original study were recruited with letters and called and the patients who did not reply or who were not followed up were excluded. Every patient underwent a complete ophthalmological evaluation and electronystagmographic recording. Visual acuities were measured monocularly and binocularly for distance and Snellen lines were used for comparison as in the original study the results were with Snellen chart. The electronystagmography instrument was the same instrument used in the original study (ICS Medical Electronystagmography N-500). Patients were asked to fixate on a distant target (approximately 3 meters) binocularly during recordings and the recordings were taken at straight-ahead position and 10 and 20 degrees lateral gazes. The amplitude of the nystagmus (degrees) was defined as the peak-to-peak slow phase displacement, frequency was defined as the number of oscillations per second (oscillations/sec), and intensity (degree/sec) was calculated as the product of amplitude and frequency. Stereopsis was measured with Randot Stereotests (Stereo Optical Co., Inc., Chicago, Illinois). Besides objective measurements with electronystagmography, subjective results were obtained by asking patients and parents about their impressions and observations related to the surgery since the initial surgery. Exclusion criteria for patients were the presence of other ocular structural anomalies or diseases such as cataract, glaucoma, or treatments for eye diseases and failure to follow-up. Since our publication, the classification of nystagmus has been changed, and for this study we used the classification of National Eye Institute (Classification of eye movement abnormalities and strabismus (CEMAS), 2001).4 All of our patients were accepted in the group of INS and classification as motor and sensory was abandoned according to the clasification given in CEMAS. Diagnosis, age, and sex characteristics of the patients are given in Table 1.
1 2 3 4 5 6
(M) (M) (M) (M) (F) (M)
Diagnosis
Age at operation (years)
Age at last visit (years)
Cone dystrophy Cone dystrophy Albinism Degenerative myopia Idiopathic Idiopathic
7 8 7 14 7 6
24 22 21 28 20 20
TABLE 2. The best corrected visual acuities (VA) that were measured preoperatively (preop), postoperatively (postop), and at the final visit as well as binocular acuity are shown. Patient no 1 2 3 4 5 6
Preop VA
Postop VA
Final VA
Binocular VA
0.1/0.1 0.05/0.05 0.1/0.1 0.3/0.3 0.5/0.5 0.3/04
0.1/0.1 0.1/0.1 0.3/0.3 0.3/0.4 0.8/0.8 0.6/0.6
0.1/0.1 0.05/0.05 0.4/0.3 0.4/0.4 0.9/0.8 0.8/1.0
0.1 0.1 0.4 0.4 0.9 1.0
RESULTS In our previous paper, the mean follow-up period was about 22 months (max 36 months) and mean age of the patients at the time of operation was 8.5 years. Mean follow-up period for the current study is 14.17 ± 0.41 years (min: 14, max: 15 years), and the mean age at the final visit was 22.67 ± 2.94 years (min: 20, max: 28 years). According to our original data, there was a 1.2-line increase in visual acuity after four horizontal rectus muscle recession in about 2 years follow-up period. Current study showed that this increase was sustained in all patients till the last visit. Preoperative visual acuities, the acuities after surgery and the final measurements at the last follow-up visit are shown in Table 2. The increase in visual acuity (the final visual acuity in comparison to preoperative visual acuity) in terms of Snellen lines was 2.17 for the right eye (ranging between 0 to 5 lines) and 2.0 for the left eye (ranging between 0 to 6 lines). When we compared the final visual acuity with the postoperative visual acuity, the change was 0.75 Snellen lines for the right eye and 0.67 Snellen lines for the left eye. Mean changes in visual acuities for each eye are given in Table 3. When we compared the results with Wilcoxon signed ranks test, there was no statistical significance inspite of the 2.17 lines increase for the right and 2.0 lines increase for the left eye (right eye visual acuity preoperative and final: z = 1.826, p = 0.068; Strabismus
Long-term results of nystagmus surgery TABLE 3. The mean visual acuities for right and left eyes and the objective measurements (nystagmus frequency, amplitude, and intensity) that were performed before and after surgery and at the last visit (n = 6). Final results PrePost(mean follow-up operative operative 14 years)
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Mean visual acuity –right eye Mean visual acuity – left eye Nystagmus frequency Nystagmus amplitude Nystagmus intensity
0.23
0.37
0.44
0.24
0.40
0.44
3.73 9.22 32.08
3.15 4.30 11.80
2.55 3.58 9.20
postoperative and final: z = 1.786, p = 0.074, respectively; left eye visual acuity preoperative and final: z = 1.826, p = 0.068; postperative and final: z = 0.00, p = 1.0, respectively). Five of the patients were orthophoric and one patient had exophoria of 16 prism diopters (PD) postoperatively with a very good control; none of the cases had any associated restriction or muscle dysfunction after surgery. For objective evaluation we had electronystagmography recordings. When the nystagmus frequency was evaluated, even though the decrease in the postoperative period was significant (Wilcoxon signed ranks test z = 1.992, p = 0.046), the decrease in final visit was statistically insignificant (Wilcoxon signed ranks test, z = 1.153, p = 0.249). The decrease in nystagmus amplitude compared to the preoperative values both postoperatively and in the long-term follow-up was statistically significant (z = 2.201, p = 0.028, and z = 2.207, p = 0.027, respectively). The change of nystagmus amplitude between the postoperative visit and the final visit (approximately 12 years) was insignificant (z = 1.153, p = 0.249). Similar statistical results were detected for nystagmus intensity as well. The decrease in intensity between preoperative and postoperative values and preoperative and long-term values was significant (z = 2.201, p = 0.028; z = 2.201, p = 0.028), however the decrease that was detected at the final control was insignificant (z = 0.944, p = 0.345) (Table 3). When stereopsis values were compared, there was no significant change after surgery (preoperative and postoperative median stereopsis values were 600 sec arc). However at the long-term final visit the median stereopsis value was 200 sec of arc, and the main improvement in long-term follow-up was in the stereopsis values (preoperative and final stereopsis, z = 2.013, p = 0.043, postoperative and final stereopsis z = 2.013, p = 0.043). The stereopsis values are given in Table 4. For subjective evaluation, at the final examination patients or parents were asked whether they were satisfied with the results and whether they would !
2014 Informa Healthcare USA, Inc.
83
TABLE 4. Stereopsis values (sec arc) of the patients preoperatively, postoperatively, and at the final visit. Patient no 1 2 3 4 5 6 Median
Preop stereopsis
Postop stereopsis
Final stereopsis
800 800 3000 400 80 100
800 800 3000 400 50 100
200 400 3000 200 40 50
600 sec arc
600 sec arc
200 sec arc
have this surgery performed if they were asked again. Two-thirds of the patients were satisfied with the result of the surgery and would have the same surgery if they were asked again. Head posture was not detected in 3 patients and was still present in 3 patients but the parents and the patients thought that it was better compared to the presurgical situation.
DISCUSSION In this retrospective study, we may conclude that beneficial effects of the four muscle recession have been maintained during the time interval since our initial report.3 Our impression was the deteroriation of the initial improvement with time, especially after an infection or psychological trauma, and in order to investigate we decided to analyze the findings over the long term. However, the clinical findings and electronystagmographic recordings showed that changes in visual acuity and decrease in intensity persisted in long-term follow-up and even further improvement in stereopsis was achieved. Even though increase in visual acuity was not statistically significant due to the small number of patients, the improvement in stereopsis was detected in all cases except one. In general, stereoacuity test scores improve with age, whereas performance variability decreases with age and normal adult findings are usually achieved by age 7. Improvement in median stereopsis was accepted in relation to stabilization of nystagmus with longer follow-up, however learning effect couldn’t be neglected. As there is no definitive cure for infantile nystagmus, the main aim of the treatment is to correct the refractive errors and strabismus if present, and to achieve optimal development of visual system in the sensitive period. Correction of refractive errors helps to get a clearer image on fovea diminishing the adverse effects of blurred vision. The correction of strabismus improves the binocular vision and this helps to keep the eyes aligned so that the intensity of nystagmus decreases. Surgical treatment for nystagmus is extensively and well documented in the
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84 H. Atilla et al. literature and there are many reports for the benefits of surgery.2,3,5–12 Surgery in nystagmus is usually performed to correct head posture and strabismus and to improve vision by decreasing nystagmus amplitude to increase foveation time. The patients with good binocular function and alignment in primary position are not accepted as candidates for surgery generally. The main outcome of surgery is to have decrease in nystagmus frequency and intensity, and improvement in head posture and visual acuity secondarily. As reviewed by Hertle, almost all of the studies were uncontrolled case series.13 Surgery was mostly done to improve head posture. Most of the authors concluded that nystagmus decreased and visual acuity improved by surgical intervention. However it is important to know the long-term stability of the improved results after surgery to assess the predictability of the surgical results. There are reports in literature about different success rates of four horizontal muscle recession surgery, however the longest follow-up period was about 2.5 years.9,14,15 In this study, we aimed to have the objective and subjective evaluations of these patients for a longer follow-up period (minimum 14 years). As previously stated in various studies, one of the most common features of the infantile nystagmus waveforms is the presence of the slow phase, wherein the eyes remain at or close to the point of desired fixation with little or no movement, called ‘‘foveation periods’’ to enhance visual acuity.1–4,10 The duration of foveation is directly related to visual acuity and four horizontal rectus muscle recession surgery can help to extend these periods so that visual acuity may increase secondarily. Sprunger and colleagues assessed the effect of four muscle recession on recognition time and concluded that surgery decreased the time necessary to recognize optoptypes and improved visual function.16 ElKamshoushy and colleagues reported significant postoperative improvement in visual acuity and recognition time. They suggested that recognition time used in their study simulated natural viewing conditions and allowed the clinician and patient to understand better and appreciate the effect of the surgery.17 In some reports, these outcomes have been shown with objective measurements such as eye movement recordings with electronystagmography. It was suggested that amplitude is not a good indicator of visual acuity, and rather than merely the amplitudes or frequencies, the quality of the nystagmus is more important. However the relationship among Snellen visual acuity, nystagmus, and other sensory visual functions is complex and the visual acuity may not increase in proportion to the recordings.1 The effect on vision of changing a patient’s nystagmus is related to a number of unknown, unpredictable variables, including patient age, underlying visual sensory system disease, associated strabismus, associated
amblyopia, uncorrected refractive errors, and associated central nervous system disease. The accuracy and duration of foveation have been directly linked to visual acuity, especially in patients in whom no other sensory system disease can be found.1,18 In our patients, increase in visual acuity was more significant in idiopathic cases (cases 5 and 6) and no improvement was detected in cone dystrophy cases Previous eye muscle studies with electron microscopy revealed variable anomalous enthesial nerve endings as well as anomalous vascular endothelial cells in INS patients. This was reported to be related to immaturity of postnatal development of neurovascular complexes specific to the ocular motor disorders.19 Tenotomy was reported to have dramatic effect on nystagmus due to recently discovered nerve endings in the extraocular muscles at the tendino-scleral interface (enthesis). The tenotomy and reattachment procedure was first described by Dell’Osso et al. on achiasmatic canines.6,20 The clinical and electrophysiologic consequences of extraocular muscle tenotomy in patients with nystagmus may be due to interruption of the afferent proprioceptive loop, producing a damped peripheral ocular-motor response to the nystagmus signal.1,2,6 The positive effect of four horizontal rectus muscle recession surgery may be related to the tenotomy performed, but it is hard to comment on whether this surgery would be effective without recession. We do not know if the success is merely due to tenotomy or whether the recession procedure has an additional beneficial effect by decreasing the arc of muscle on the globe. It was also suggested that patients with INS may be particularly prone to the placebo effect as they are highly motivated and may improve with repeated measurements due to decreased stress, and even surgical intervention can have placebo effects.13 However, in our cases, we were able to show the improvement objectively in addition to subjective patient satisfaction. Two-thirds of the patients and parents would have the surgery if they were asked again and reported that they were satisfied with the result of the surgery, however, there could be potential bias related to direct questioning. Correction of associated strabismus would have an additive effect on visual acuity. However, we could not comment on this, as all of our cases were orthophoric except one with exophoria with good control (case 6). In patients with associated strabismus, establishment of binocular vision may help achieving decreased nystagmus amplitude and frequency with secondary increase in visual acuity. The restrictions of this study is retrospective design, absence of a control group, and the small number of patients that are included. Foveation time measurement could have been more appropiate for INS patients for objective outcome of surgery, however to be consistent with the previous paper and to Strabismus
Long-term results of nystagmus surgery
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be able to compare the results we preferred electronystagmography parameters such as frequency and amplitude.21,22 Only half of the patients from previous study were included in the recent study according to the longer follow-up criteria for inclusion. In conclusion, we may suggest that four horizontal rectus muscle surgery has beneficial effects on visual acuity and binocular functions in the long term. However the effect is difficult to explain, whether due to decreased arc effect of the muscle or due to the tenotomy of the muscle that was performed during recession. It would be beneficiary to conduct a study comparing the four horizontal rectus muscle surgery and tenotomy that would be performed randomly.
DECLARATION OF INTEREST The authors report no conflicts of interest.
REFERENCES 1. Hertle RW, Dell’Osso LF, FitzGibbon EJ, et al. Horizontal rectus tenotomy in patients with congenital nystagmus. Ophthalmology 2003;110:2097–2105. 2. Hertle RW, Anninger W, Yang D, et al. Effects of extraocular muscle surgery on 15 patients with oculocutaneous albinism (OCA) and infantile nystagmus syndrome. Am J Ophthalmol 2004;138:978–987. 3. Atilla H, I¸s ıkc¸elik Y, Erkam N. Surgical treatment in nystagmus. Eye 1999;13:11–15. 4. CEMAS working group. A National Eye Institute sponsored workshop and publication on the classification of eye movement abnormalities and strabismus (CEMAS). In: The National Eye Institute Publications. Bethesda MD. 2001. 5. Biglan AW, Hiles DA, Ying-Fen Z, et al. Results after surgery for null point nystgamus with abnormal head position. Am Orthoptic J 1989;39:134–142. 6. Dell’Osso LF. Extraocular muscle tenotomy, dissection and suture: a hypothetical therapy for congenital nystagmus. J Pediatr Ophthalmol Strabismus 1998;35:232–233.
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7. Dell’Osso LF, Flynn JT. Congenital nystagmus surgery: a quantitative evaluation of the effects. Arch Ophthalmol 1979;97:462–469. 8. Flynn JT, Dell’Osso LF. The effects of congenital nystagmus surgery. Ophthalmology 1970;86:1414–1427. 9. Helveston EM, Ellis FD, Plager DA. Larger recession of the horizontal recti for treatment of nystagmus. Ophthalmology 1991;98:1302–1305. 10. Hertle RW, Dell’Osso LF, FitzGibbon EJ, et al. Horizontal rectus muscle tenotomy in children with infantile nystagmus syndrome: A pilot study. J AAPOS 2004;8:539–548. 11. Pratt-Johnson JA. The surgery of congenital nystagmus. Can J Ophthalmol 1971;6:268–272. 12. Scott WE, Kraft SP. Surgical treatment of compensatory head position in congenital nystagmus. J Pediatr Ophthalmol Strabismus 1984;21:85–95. 13. Hertle RW. Nystagmus in infancy and childhood: Characteristics and evidence for treatment. Am Orthoptic J 2010;60:48–58. 14. Boyle NJ, Dawson EL, Lee JP. Benefits of retroequatorial four horizontal muscle recession in congenital idiopathic nystagmus in adults. J AAPOS 2006;10:404–408. 15. von Noorden GK, Sprunger DT. Large rectus muscle recessions for the treatment of congenital nystagmus. Arch Ophthalmol 1991;109:221–224. 16. Sprunger DT, Fahad B, Helveston EM. Recognition time after four muscle recession for nystagmus. Am Orthoptic J 1997;47:122–125. 17. ElKamshoushy A, Shawky D, ElMassry A, et al. Improved visual acuity and recognition time in nystagmus patients following four-muscle recession or Kestenbaum-Anderson procedures. J AAPOS 2012;16:36–40. 18. Dell’Osso LF, van der Steen J, Steinman RM, Collewijn H. Foveation dynamics in congenital nystagmus. I:Fixation. Doc Ophthalmolo 1992;79:1–23. 19. Hertle RW, Chan CC, Galita DA, et al. Neuroanatomy of the extraocular muscle tendon enthesis in macaque, normal human, and patients with congenital nystagmus. J AAPOS 2002;6:319–327. 20. Dell’Osso LF, Hertle RW, Williams RW, Jacobs JB. A new surgery for congenital nystgamus: effects of tenotomy on an achiasmatic canine and the role of extraocular proprioception. J AAPOS 1999;3:166–182. 21. Hertle RW, Dell’Osso LF. Clinical and ocular motor analysis of congenital nystagmus in infancy. J AAPOS 1999;3:70–79. 22. Hertle RW, Yang D, Tai Z, et al. A systmeatic approach to eye muscle surgery for infantile nystagmus syndrome: results in 100 patients. Binocul Vis Strabismus Q 2010;25: 72–93.
Long-term results of four horizontal rectus muscle recession in nystagmus treatment Huban Atilla,
Strabismus Downloaded from informahealthcare.com by Baylor University on 06/28/14 For personal use only.
1
1
MD
, Helin Deniz Demir,
MD
2
, and Yusuf I¸s ıkc¸elik,
MD
3
Faculty of Medicine, Department of Ophthalmology, Ankara University, Ankara, Turkey, 2Faculty of Medicine, Department of Ophthalmology, Tokat Gaziosmanpa¸sa University, Tokat, Turkey, and 3U¸sak Eye Center, U¸sak, Turkey
ABSTRACT Purpose: To report the long-term results of four horizontal rectus muscle recessions that were performed for infantile nystagmus syndrome treatment. Methods: In this case series, patients with infantile nystagmus syndrome who had four horizontal muscle recessions previously were recruited and ophthalmological examination and electronystagmography recordings were performed. Objectively, amplitude and frequency of nystagmus were measured from the recordings and the intensity was calculated. Visual acuity, stereopsis, and alignment were evaluated and compared with the preoperative and postoperative values. Results: The records of the 12 patients who had four horizontal rectus muscle recession surgery were evaluated and six patients (5 male, 1 female) who had regular follow-ups were included in this study. Mean follow-up was 14.17 ± 0.41 years (minimum 14 years, maximum 15 years) and mean age of patients at the last visit was 22 years (20-28 years). On subjective evaluation, two-thirds (4/6) of the patients were satisfied with the surgical results and had the impression that after surgery, nystagmus decreased in intensity and head posture improved. On objective evaluation, visual acuity was found to be the same, however, stereopsis improved (preoperatively and postoperatively median stereopsis was 600 sec arc vs 200 sec arc final). The decrease in nystagmus amplitude and frequency was still maintained. Conclusions: Nystagmus surgery on four horizontal rectus muscles has positive effects on binocular function and nystagmus parameters in the long-term follow-up. As we could not treat the primary pathology, the visual acuity was about the same but the decrease in nystagmus amplitude and frequency was still maintained with better stereopsis, and patient satisfaction. Keywords: Electronystagmography, infantile nystagmus syndrome, nystagmus, nystagmus surgery
INTRODUCTION
treatment modality for INS due to associated visual sensory system abnormalities or inherited underlying defects. Therefore the main goal of the treatment for nystagmus is usually to reduce the intensity of the nystagmus in order to increase foveation time or to shift the gaze position with the lowest nystagmus frequency (null zone) to the primary position and to decrease or eliminate head posture. There are different surgical treatment modalities that are widely known such as Anderson-Kestenbaum, Anderson, four horizontal rectus muscle recession, or tenotomy
Infantile nystagmus syndrome (INS) is an ocularmotor disorder of unknown etiology that presents at birth or early infancy and is clinically characterized by involuntary oscillations of the eyes.1,2 Estimations of the incidence of INS vary from 0.03% to 0.0005%; the generally accepted figure is 0.015%. Patients with INS usually have diminished visual acuity and this may be inversely related to the intensity of the nystagmus.1 Unfortunately there is no radical or highly effective
Received 23 May 2013; Revised 13 November 2013; Accepted 5 February 2014; Published online 28 April 2014 Correspondence: Prof Dr Huban Atilla, Faculty of Medicine, Department of Ophthalmology, Ankara University, Mamak cad no: 4 Dikimevi _ ¨ RKIYE. Ankara, 06260 TU Tel: 90 532 4541604. Fax: 90 312 466 66 31. E-mail: [email protected]
81
82 H. Atilla et al. of the recti, however long-term effects are not definitely described. The aim of this study is to report the long-term results of four muscle recession in infantile nystagmus syndrome patients.
TABLE 1. The gender and diagnosis of the patients and their ages at the time of operation and at the time of last visit (M: male, F: female). Patient # (sex)
Strabismus Downloaded from informahealthcare.com by Baylor University on 06/28/14 For personal use only.
MATERIALS AND METHODS The results of the initial study were published previously.3 The records of the 12 patients who had nystagmus surgery were evaluated and 6 patients (5 male, 1 female) who had regular follow-ups were included in the current study. All procedures followed the declaration of Helsinki and informed consent forms were filled out and signed by the parents or patients. For inclusion in the study, the patients who had a follow-up period of at least 10 years were included. All of the patients in the original study were recruited with letters and called and the patients who did not reply or who were not followed up were excluded. Every patient underwent a complete ophthalmological evaluation and electronystagmographic recording. Visual acuities were measured monocularly and binocularly for distance and Snellen lines were used for comparison as in the original study the results were with Snellen chart. The electronystagmography instrument was the same instrument used in the original study (ICS Medical Electronystagmography N-500). Patients were asked to fixate on a distant target (approximately 3 meters) binocularly during recordings and the recordings were taken at straight-ahead position and 10 and 20 degrees lateral gazes. The amplitude of the nystagmus (degrees) was defined as the peak-to-peak slow phase displacement, frequency was defined as the number of oscillations per second (oscillations/sec), and intensity (degree/sec) was calculated as the product of amplitude and frequency. Stereopsis was measured with Randot Stereotests (Stereo Optical Co., Inc., Chicago, Illinois). Besides objective measurements with electronystagmography, subjective results were obtained by asking patients and parents about their impressions and observations related to the surgery since the initial surgery. Exclusion criteria for patients were the presence of other ocular structural anomalies or diseases such as cataract, glaucoma, or treatments for eye diseases and failure to follow-up. Since our publication, the classification of nystagmus has been changed, and for this study we used the classification of National Eye Institute (Classification of eye movement abnormalities and strabismus (CEMAS), 2001).4 All of our patients were accepted in the group of INS and classification as motor and sensory was abandoned according to the clasification given in CEMAS. Diagnosis, age, and sex characteristics of the patients are given in Table 1.
1 2 3 4 5 6
(M) (M) (M) (M) (F) (M)
Diagnosis
Age at operation (years)
Age at last visit (years)
Cone dystrophy Cone dystrophy Albinism Degenerative myopia Idiopathic Idiopathic
7 8 7 14 7 6
24 22 21 28 20 20
TABLE 2. The best corrected visual acuities (VA) that were measured preoperatively (preop), postoperatively (postop), and at the final visit as well as binocular acuity are shown. Patient no 1 2 3 4 5 6
Preop VA
Postop VA
Final VA
Binocular VA
0.1/0.1 0.05/0.05 0.1/0.1 0.3/0.3 0.5/0.5 0.3/04
0.1/0.1 0.1/0.1 0.3/0.3 0.3/0.4 0.8/0.8 0.6/0.6
0.1/0.1 0.05/0.05 0.4/0.3 0.4/0.4 0.9/0.8 0.8/1.0
0.1 0.1 0.4 0.4 0.9 1.0
RESULTS In our previous paper, the mean follow-up period was about 22 months (max 36 months) and mean age of the patients at the time of operation was 8.5 years. Mean follow-up period for the current study is 14.17 ± 0.41 years (min: 14, max: 15 years), and the mean age at the final visit was 22.67 ± 2.94 years (min: 20, max: 28 years). According to our original data, there was a 1.2-line increase in visual acuity after four horizontal rectus muscle recession in about 2 years follow-up period. Current study showed that this increase was sustained in all patients till the last visit. Preoperative visual acuities, the acuities after surgery and the final measurements at the last follow-up visit are shown in Table 2. The increase in visual acuity (the final visual acuity in comparison to preoperative visual acuity) in terms of Snellen lines was 2.17 for the right eye (ranging between 0 to 5 lines) and 2.0 for the left eye (ranging between 0 to 6 lines). When we compared the final visual acuity with the postoperative visual acuity, the change was 0.75 Snellen lines for the right eye and 0.67 Snellen lines for the left eye. Mean changes in visual acuities for each eye are given in Table 3. When we compared the results with Wilcoxon signed ranks test, there was no statistical significance inspite of the 2.17 lines increase for the right and 2.0 lines increase for the left eye (right eye visual acuity preoperative and final: z = 1.826, p = 0.068; Strabismus
Long-term results of nystagmus surgery TABLE 3. The mean visual acuities for right and left eyes and the objective measurements (nystagmus frequency, amplitude, and intensity) that were performed before and after surgery and at the last visit (n = 6). Final results PrePost(mean follow-up operative operative 14 years)
Strabismus Downloaded from informahealthcare.com by Baylor University on 06/28/14 For personal use only.
Mean visual acuity –right eye Mean visual acuity – left eye Nystagmus frequency Nystagmus amplitude Nystagmus intensity
0.23
0.37
0.44
0.24
0.40
0.44
3.73 9.22 32.08
3.15 4.30 11.80
2.55 3.58 9.20
postoperative and final: z = 1.786, p = 0.074, respectively; left eye visual acuity preoperative and final: z = 1.826, p = 0.068; postperative and final: z = 0.00, p = 1.0, respectively). Five of the patients were orthophoric and one patient had exophoria of 16 prism diopters (PD) postoperatively with a very good control; none of the cases had any associated restriction or muscle dysfunction after surgery. For objective evaluation we had electronystagmography recordings. When the nystagmus frequency was evaluated, even though the decrease in the postoperative period was significant (Wilcoxon signed ranks test z = 1.992, p = 0.046), the decrease in final visit was statistically insignificant (Wilcoxon signed ranks test, z = 1.153, p = 0.249). The decrease in nystagmus amplitude compared to the preoperative values both postoperatively and in the long-term follow-up was statistically significant (z = 2.201, p = 0.028, and z = 2.207, p = 0.027, respectively). The change of nystagmus amplitude between the postoperative visit and the final visit (approximately 12 years) was insignificant (z = 1.153, p = 0.249). Similar statistical results were detected for nystagmus intensity as well. The decrease in intensity between preoperative and postoperative values and preoperative and long-term values was significant (z = 2.201, p = 0.028; z = 2.201, p = 0.028), however the decrease that was detected at the final control was insignificant (z = 0.944, p = 0.345) (Table 3). When stereopsis values were compared, there was no significant change after surgery (preoperative and postoperative median stereopsis values were 600 sec arc). However at the long-term final visit the median stereopsis value was 200 sec of arc, and the main improvement in long-term follow-up was in the stereopsis values (preoperative and final stereopsis, z = 2.013, p = 0.043, postoperative and final stereopsis z = 2.013, p = 0.043). The stereopsis values are given in Table 4. For subjective evaluation, at the final examination patients or parents were asked whether they were satisfied with the results and whether they would !
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TABLE 4. Stereopsis values (sec arc) of the patients preoperatively, postoperatively, and at the final visit. Patient no 1 2 3 4 5 6 Median
Preop stereopsis
Postop stereopsis
Final stereopsis
800 800 3000 400 80 100
800 800 3000 400 50 100
200 400 3000 200 40 50
600 sec arc
600 sec arc
200 sec arc
have this surgery performed if they were asked again. Two-thirds of the patients were satisfied with the result of the surgery and would have the same surgery if they were asked again. Head posture was not detected in 3 patients and was still present in 3 patients but the parents and the patients thought that it was better compared to the presurgical situation.
DISCUSSION In this retrospective study, we may conclude that beneficial effects of the four muscle recession have been maintained during the time interval since our initial report.3 Our impression was the deteroriation of the initial improvement with time, especially after an infection or psychological trauma, and in order to investigate we decided to analyze the findings over the long term. However, the clinical findings and electronystagmographic recordings showed that changes in visual acuity and decrease in intensity persisted in long-term follow-up and even further improvement in stereopsis was achieved. Even though increase in visual acuity was not statistically significant due to the small number of patients, the improvement in stereopsis was detected in all cases except one. In general, stereoacuity test scores improve with age, whereas performance variability decreases with age and normal adult findings are usually achieved by age 7. Improvement in median stereopsis was accepted in relation to stabilization of nystagmus with longer follow-up, however learning effect couldn’t be neglected. As there is no definitive cure for infantile nystagmus, the main aim of the treatment is to correct the refractive errors and strabismus if present, and to achieve optimal development of visual system in the sensitive period. Correction of refractive errors helps to get a clearer image on fovea diminishing the adverse effects of blurred vision. The correction of strabismus improves the binocular vision and this helps to keep the eyes aligned so that the intensity of nystagmus decreases. Surgical treatment for nystagmus is extensively and well documented in the
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84 H. Atilla et al. literature and there are many reports for the benefits of surgery.2,3,5–12 Surgery in nystagmus is usually performed to correct head posture and strabismus and to improve vision by decreasing nystagmus amplitude to increase foveation time. The patients with good binocular function and alignment in primary position are not accepted as candidates for surgery generally. The main outcome of surgery is to have decrease in nystagmus frequency and intensity, and improvement in head posture and visual acuity secondarily. As reviewed by Hertle, almost all of the studies were uncontrolled case series.13 Surgery was mostly done to improve head posture. Most of the authors concluded that nystagmus decreased and visual acuity improved by surgical intervention. However it is important to know the long-term stability of the improved results after surgery to assess the predictability of the surgical results. There are reports in literature about different success rates of four horizontal muscle recession surgery, however the longest follow-up period was about 2.5 years.9,14,15 In this study, we aimed to have the objective and subjective evaluations of these patients for a longer follow-up period (minimum 14 years). As previously stated in various studies, one of the most common features of the infantile nystagmus waveforms is the presence of the slow phase, wherein the eyes remain at or close to the point of desired fixation with little or no movement, called ‘‘foveation periods’’ to enhance visual acuity.1–4,10 The duration of foveation is directly related to visual acuity and four horizontal rectus muscle recession surgery can help to extend these periods so that visual acuity may increase secondarily. Sprunger and colleagues assessed the effect of four muscle recession on recognition time and concluded that surgery decreased the time necessary to recognize optoptypes and improved visual function.16 ElKamshoushy and colleagues reported significant postoperative improvement in visual acuity and recognition time. They suggested that recognition time used in their study simulated natural viewing conditions and allowed the clinician and patient to understand better and appreciate the effect of the surgery.17 In some reports, these outcomes have been shown with objective measurements such as eye movement recordings with electronystagmography. It was suggested that amplitude is not a good indicator of visual acuity, and rather than merely the amplitudes or frequencies, the quality of the nystagmus is more important. However the relationship among Snellen visual acuity, nystagmus, and other sensory visual functions is complex and the visual acuity may not increase in proportion to the recordings.1 The effect on vision of changing a patient’s nystagmus is related to a number of unknown, unpredictable variables, including patient age, underlying visual sensory system disease, associated strabismus, associated
amblyopia, uncorrected refractive errors, and associated central nervous system disease. The accuracy and duration of foveation have been directly linked to visual acuity, especially in patients in whom no other sensory system disease can be found.1,18 In our patients, increase in visual acuity was more significant in idiopathic cases (cases 5 and 6) and no improvement was detected in cone dystrophy cases Previous eye muscle studies with electron microscopy revealed variable anomalous enthesial nerve endings as well as anomalous vascular endothelial cells in INS patients. This was reported to be related to immaturity of postnatal development of neurovascular complexes specific to the ocular motor disorders.19 Tenotomy was reported to have dramatic effect on nystagmus due to recently discovered nerve endings in the extraocular muscles at the tendino-scleral interface (enthesis). The tenotomy and reattachment procedure was first described by Dell’Osso et al. on achiasmatic canines.6,20 The clinical and electrophysiologic consequences of extraocular muscle tenotomy in patients with nystagmus may be due to interruption of the afferent proprioceptive loop, producing a damped peripheral ocular-motor response to the nystagmus signal.1,2,6 The positive effect of four horizontal rectus muscle recession surgery may be related to the tenotomy performed, but it is hard to comment on whether this surgery would be effective without recession. We do not know if the success is merely due to tenotomy or whether the recession procedure has an additional beneficial effect by decreasing the arc of muscle on the globe. It was also suggested that patients with INS may be particularly prone to the placebo effect as they are highly motivated and may improve with repeated measurements due to decreased stress, and even surgical intervention can have placebo effects.13 However, in our cases, we were able to show the improvement objectively in addition to subjective patient satisfaction. Two-thirds of the patients and parents would have the surgery if they were asked again and reported that they were satisfied with the result of the surgery, however, there could be potential bias related to direct questioning. Correction of associated strabismus would have an additive effect on visual acuity. However, we could not comment on this, as all of our cases were orthophoric except one with exophoria with good control (case 6). In patients with associated strabismus, establishment of binocular vision may help achieving decreased nystagmus amplitude and frequency with secondary increase in visual acuity. The restrictions of this study is retrospective design, absence of a control group, and the small number of patients that are included. Foveation time measurement could have been more appropiate for INS patients for objective outcome of surgery, however to be consistent with the previous paper and to Strabismus
Long-term results of nystagmus surgery
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be able to compare the results we preferred electronystagmography parameters such as frequency and amplitude.21,22 Only half of the patients from previous study were included in the recent study according to the longer follow-up criteria for inclusion. In conclusion, we may suggest that four horizontal rectus muscle surgery has beneficial effects on visual acuity and binocular functions in the long term. However the effect is difficult to explain, whether due to decreased arc effect of the muscle or due to the tenotomy of the muscle that was performed during recession. It would be beneficiary to conduct a study comparing the four horizontal rectus muscle surgery and tenotomy that would be performed randomly.
DECLARATION OF INTEREST The authors report no conflicts of interest.
REFERENCES 1. Hertle RW, Dell’Osso LF, FitzGibbon EJ, et al. Horizontal rectus tenotomy in patients with congenital nystagmus. Ophthalmology 2003;110:2097–2105. 2. Hertle RW, Anninger W, Yang D, et al. Effects of extraocular muscle surgery on 15 patients with oculocutaneous albinism (OCA) and infantile nystagmus syndrome. Am J Ophthalmol 2004;138:978–987. 3. Atilla H, I¸s ıkc¸elik Y, Erkam N. Surgical treatment in nystagmus. Eye 1999;13:11–15. 4. CEMAS working group. A National Eye Institute sponsored workshop and publication on the classification of eye movement abnormalities and strabismus (CEMAS). In: The National Eye Institute Publications. Bethesda MD. 2001. 5. Biglan AW, Hiles DA, Ying-Fen Z, et al. Results after surgery for null point nystgamus with abnormal head position. Am Orthoptic J 1989;39:134–142. 6. Dell’Osso LF. Extraocular muscle tenotomy, dissection and suture: a hypothetical therapy for congenital nystagmus. J Pediatr Ophthalmol Strabismus 1998;35:232–233.
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7. Dell’Osso LF, Flynn JT. Congenital nystagmus surgery: a quantitative evaluation of the effects. Arch Ophthalmol 1979;97:462–469. 8. Flynn JT, Dell’Osso LF. The effects of congenital nystagmus surgery. Ophthalmology 1970;86:1414–1427. 9. Helveston EM, Ellis FD, Plager DA. Larger recession of the horizontal recti for treatment of nystagmus. Ophthalmology 1991;98:1302–1305. 10. Hertle RW, Dell’Osso LF, FitzGibbon EJ, et al. Horizontal rectus muscle tenotomy in children with infantile nystagmus syndrome: A pilot study. J AAPOS 2004;8:539–548. 11. Pratt-Johnson JA. The surgery of congenital nystagmus. Can J Ophthalmol 1971;6:268–272. 12. Scott WE, Kraft SP. Surgical treatment of compensatory head position in congenital nystagmus. J Pediatr Ophthalmol Strabismus 1984;21:85–95. 13. Hertle RW. Nystagmus in infancy and childhood: Characteristics and evidence for treatment. Am Orthoptic J 2010;60:48–58. 14. Boyle NJ, Dawson EL, Lee JP. Benefits of retroequatorial four horizontal muscle recession in congenital idiopathic nystagmus in adults. J AAPOS 2006;10:404–408. 15. von Noorden GK, Sprunger DT. Large rectus muscle recessions for the treatment of congenital nystagmus. Arch Ophthalmol 1991;109:221–224. 16. Sprunger DT, Fahad B, Helveston EM. Recognition time after four muscle recession for nystagmus. Am Orthoptic J 1997;47:122–125. 17. ElKamshoushy A, Shawky D, ElMassry A, et al. Improved visual acuity and recognition time in nystagmus patients following four-muscle recession or Kestenbaum-Anderson procedures. J AAPOS 2012;16:36–40. 18. Dell’Osso LF, van der Steen J, Steinman RM, Collewijn H. Foveation dynamics in congenital nystagmus. I:Fixation. Doc Ophthalmolo 1992;79:1–23. 19. Hertle RW, Chan CC, Galita DA, et al. Neuroanatomy of the extraocular muscle tendon enthesis in macaque, normal human, and patients with congenital nystagmus. J AAPOS 2002;6:319–327. 20. Dell’Osso LF, Hertle RW, Williams RW, Jacobs JB. A new surgery for congenital nystgamus: effects of tenotomy on an achiasmatic canine and the role of extraocular proprioception. J AAPOS 1999;3:166–182. 21. Hertle RW, Dell’Osso LF. Clinical and ocular motor analysis of congenital nystagmus in infancy. J AAPOS 1999;3:70–79. 22. Hertle RW, Yang D, Tai Z, et al. A systmeatic approach to eye muscle surgery for infantile nystagmus syndrome: results in 100 patients. Binocul Vis Strabismus Q 2010;25: 72–93.
