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The effect of neutral density lters on testing in patients with strabismic amblyopia Syed Yaser Habeeb, MD, Brian W. Arthur, MD, Martin W. ten Hove, MD, MEng ABSTRACT   RÉSUMÉ Objective: To confirm if using a neutral density filter (NDF) affects eyes with strabismic amblyopia differently compared to fellow non-amblyopic eyes, and to determine if a similar effect could be observed when using a NDF during peripheral visual field testing. Design: Prospective controlled case series. Participants: 19 subjects with strabismic amblyopia with visual acuities between 20/400 and 20/40 in their affected eyes were recruited to the study. Fellow non-amblyopic eyes served as the control group. Methods:  Visual acuity in both eyes was assessed using a projected Snellen eye chart with two NDFs (0.4 and 3.0 densities). Visual fields wer e ass ess ed us ing a Hum ph rey per ime ter usi ng one NDF (0 .4 de nsi ty) . Be st cor recte d vis ua l acu ity an d vis ua l fie lds we re al so recor de d. Results: When using a 3.0 NDF, visual acuity was reduced in all eyes ( p   0.0001). When using a 0.4 NDF, visual acuity was significantly improved in eyes with strabismic amblyopia compared to unfiltered conditions ( p   0.0011). There was no significant effect by NDFs on visual field testing in eyes with strabismic amblyopia or fellow non-amblyopic eyes. Conclusions: Neutral density filters affect eyes with strabismic amblyopia differently than they do non-amblyopic eyes. A significant improvement in visual acuity of eyes with strabismic amblyopia was observed when using a 0.4 NDF compared to non-amblyopic eyes. Visual acuity was reduced in amblyopic as well as non-amblyopic eyes when viewing through a 3.0 NDF. No significant change in visual fields was observed when using a 0.4 NDF in amblyopic or non-amblyopic eyes. Objet :  Confirmer si l’ut ilisa tion d’un filtr e à dens ité neutre (FDN) affecte différe mment les yeux attei nts d’un e ambl yopi e due au strabisme comparativement à l’autre œil non amblyope, et déterminer si l’on peut observer un effet similaire en utilisant un FDN pour le test du champ visuel périphérique. Nature :  Série de cas prospectifs contrôlés. Participants :  19 sujets atteints d’amblyopie due au strabisme, ayant des acuités visuelles variant entre 20/400 et 20/40 dans leurs yeux affectés, ont été retenus pour l’étude. Les autres yeux non amblyopes ont servi de groupe témoin. Méthodes :  L’acuité visuelle des deux yeux a été évaluée par projection de la charte oculaire Snellen avec deux FDN (densités de 0,4 et 3,0). Les champs visuels ont été évalués avec un périmètre Humphrey utilisant un FDN (densité 0,4). La meilleure acuité visuelle corrigée et les champs visuels ont aussi été notés. Résultats :  Avec le FDN 3,0, l’acuité visuelle était réduite dans tous les yeux ( p   0,0001). Avec le FDN 0,4, l’acuité visuelle était améliorée significativement dans les yeux atteints d’amblyopie due au strabisme comparativement aux états non filtrés ( p  0,0011). Les FDN n’avaient pas d’effet significatif sur les tests de champ visuel dans les yeux ayant une amblyopie due au strabisme ou les autres yeux non amblyopes. Conclusion :  Les filtres à dens ité neutre affectent les yeux atteint s d’amblyo pie due au stra bisme différ emment des yeux non amblyopes. Une amélioration significative de l’acuité visuelle des yeux atteints d’amblyopie due au strabisme a été observée lors de l’utilisation du FDN 0,4, comparativement aux yeux non amblyopes. L’acuité visuelle a été réduite chez les yeux amblyopes et non amblyopes lorsqu’on regardait à travers un FDN 3,0. Aucun changement significatif des champs visuels n’a été observé avec un FDN 0,4 dans les yeux amblyopes ou non amblyopes. In 1959, von Noorden and Burian demonstrated that  whe n tested wit ha neu tral density lte r (NDF), visu al acu itie s in non ambl yop ic eyes of in div idu al s wi th st rab is mic ambl yo- pia decreased, while visual acuitie s in the amblyopic eyes sta ye d the sa me or even impro ved . 1 How ev er,wh en the NDF  was plac ed before an eye tha t was amblyopi c due to an organic lesion (such as macular degeneration, optic nerve atrophy, or chorioretinitis), there was an “almost grotesque drop” in vi- sual acuity. A potential application of this observation was that one could use an NDF to differentiate between strabis- mic and organic amblyopia as a quick screening tool “before proceeding with occlusion therapy, especially when amblyo- pia is of uncertain ori gin .” 2 Von Noorden an d Bu ri an pos ite d th at their results conr med an “a mb ly opi c ey e is not at it s be st under photopic conditions,” but shows “a relativ e improve- ment of its functions under mesopic conditions.” 1 To our knowledge, the 1959 study has never been rep- licated, even though the ndings are now well accepted in most textbooks concerning pediatric and neuro-ophthal- mology. Moreover, it was unknown whether using an NDF woul d exe rt a si mi la r ef fec t du ri ng vi sual eld test ing und er mes opi c condit ions. Thu s, the obj ectives of the pre s- ent study were twofold: to conrmthe eff ect of an NDF on the central visual acuity of an eye with strabismic amblyo- pia and to determine whether a similar effect (improve- ment as assessed by the mean defect) could be observed  when measuring peripheral visual elds of eyes with stra- bismic amblyopia viewed through an NDF. Preliminary results of this study were presented at the Canadian Oph- thalmological Society annual meeting in Québec City, QC, June 2010. From the Department of Ophthalmology, Queen’s University, Kingston, Ont. Originally received Jan. 26, 2012. Final revision Jan. 26, 2012. Accepted Mar. 26, 2012 Correspondence to Martin W. ten Hove, Department of Ophthalmology, 166 Brock St., Kingston ON K7L 5G2; tenhove@queen su.ca Can J Ophthalmol  2012;4 7:348–350 0008 -4182/11/$ -see fron t matter © 2012 Canadian Ophth almol ogic al Socie ty. Published by Elsevier Inc. All rights reserved. dx.doi.or g/10.1016/j.jc jo.2012.03.0 39 348  CAN J OPHTHALMOL —VOL. 47, NO. 4, AUGUST 2012

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The effect of neutral density filters on testing in patients withstrabismic amblyopia 

Syed Yaser Habeeb, MD, Brian W. Arthur, MD, Martin W. ten Hove, MD, MEng 

ABSTRACT   ● RÉSUMÉObjective:  To confirm if using a neutral density filter (NDF) affects eyes with strabismic amblyopia differently compared to fellow

non-amblyopic eyes, and to determine if a similar effect could be observed when using a NDF during peripheral visual fieldtesting.

Design: Prospective controlled case series.Participants: 19 subjects with strabismic amblyopia with visual acuities between 20/400 and 20/40 in their affected eyes were recruited

to the study. Fellow non-amblyopic eyes served as the control group.Methods:  Visual acuity in both eyes was assessed using a projected Snellen eye chart with two NDFs (0.4 and 3.0 densities). Visual fields

were assessed using a Humphrey perimeter using one NDF (0.4 density). Best corrected visual acuity and visual fields were also recorded.Results:  When using a 3.0 NDF, visual acuity was reduced in all eyes (p     0.0001). When using a 0.4 NDF, visual acuity was

significantly improved in eyes with strabismic amblyopia compared to unfiltered conditions (p     0.0011). There was no significanteffect by NDFs on visual field testing in eyes with strabismic amblyopia or fellow non-amblyopic eyes.

Conclusions:  Neutral density filters affect eyes with strabismic amblyopia differently than they do non-amblyopic eyes. A significantimprovement in visual acuity of eyes with strabismic amblyopia was observed when using a 0.4 NDF compared to non-amblyopiceyes. Visual acuity was reduced in amblyopic as well as non-amblyopic eyes when viewing through a 3.0 NDF. No significant changein visual fields was observed when using a 0.4 NDF in amblyopic or non-amblyopic eyes.

Objet :   Confirmer si l’utilisation d’un filtre à densité neutre (FDN) affecte différemment les yeux atteints d’une amblyopie due austrabisme comparativement à l’autre œil non amblyope, et déterminer si l’on peut observer un effet similaire en utilisant un FDN pourle test du champ visuel périphérique.

Nature :  Série de cas prospectifs contrôlés.Participants : 19 sujets atteints d’amblyopie due au strabisme, ayant des acuités visuelles variant entre 20/400 et 20/40 dans leurs yeux

affectés, ont été retenus pour l’étude. Les autres yeux non amblyopes ont servi de groupe témoin.Méthodes :  L’acuité visuelle des deux yeux a été évaluée par projection de la charte oculaire Snellen avec deux FDN (densités de 0,4

et 3,0). Les champs visuels ont été évalués avec un périmètre Humphrey utilisant un FDN (densité 0,4). La meilleure acuité visuellecorrigée et les champs visuels ont aussi été notés.

Résultats :  Avec le FDN 3,0, l’acuité visuelle était réduite dans tous les yeux (p    0,0001). Avec le FDN 0,4, l’acuité visuelle étaitaméliorée significativement dans les yeux atteints d’amblyopie due au strabisme comparativement aux états non filtrés ( p  0,0011).Les FDN n’avaient pas d’effet significatif sur les tests de champ visuel dans les yeux ayant une amblyopie due au strabisme ou lesautres yeux non amblyopes.

Conclusion :  Les filtres à densité neutre affectent les yeux atteints d’amblyopie due au strabisme différemment des yeux nonamblyopes. Une amélioration significative de l’acuité visuelle des yeux atteints d’amblyopie due au strabisme a été observée lors de

l’utilisation du FDN 0,4, comparativement aux yeux non amblyopes. L’acuité visuelle a été réduite chez les yeux amblyopes et nonamblyopes lorsqu’on regardait à travers un FDN 3,0. Aucun changement significatif des champs visuels n’a été observé avec un FDN0,4 dans les yeux amblyopes ou non amblyopes.

In 1959, von Noorden and Burian demonstrated that when tested with a neutraldensityfilter (NDF), visual acuitiesin nonamblyopic eyes of individuals with strabismic amblyo-pia decreased, while visual acuities in the amblyopic eyesstayed thesame or even improved.1 However,when theNDF wasplaced before an eye that wasamblyopic due to an organiclesion (such as macular degeneration, optic nerve atrophy, or

chorioretinitis), there was an “almost grotesque drop” in vi-sual acuity. A potential application of this observation wasthat one could use an NDF to differentiate between strabis-mic and organic amblyopia as a quick screening tool “beforeproceeding with occlusion therapy, especially when amblyo-piais of uncertain origin.”2 VonNoorden and Burian positedthat their results confirmedan “amblyopic eye is notat its best

under photopic conditions,” but shows “a relativ e improve-ment of its functions under mesopic conditions.”1

To our knowledge, the 1959 study has never been rep-licated, even though the findings are now well accepted inmost textbooks concerning pediatric and neuro-ophthal-mology. Moreover, it was unknown whether using anNDF would exert a similar effect during visual field testing 

under mesopic conditions. Thus, the objectives of the pres-ent study were twofold: to confirm the effect of an NDF onthe central visual acuity of an eye with strabismic amblyo-pia and to determine whether a similar effect (improve-ment as assessed by the mean defect) could be observed when measuring peripheral visual fields of eyes with stra-bismic amblyopia viewed through an NDF.

Preliminary results of this study were presented at the Canadian Oph-thalmological Society annual meeting in Québec City, QC, June 2010.From the Department of Ophthalmology, Queen’s University, Kingston,Ont.

Originally received Jan. 26, 2012. Final revision Jan. 26, 2012. Accepted

Mar. 26, 2012

Correspondence to Martin W. ten Hove, Department of Ophthalmology,166 Brock St., Kingston ON K7L 5G2; [email protected] 

Can J Ophthalmol  2012;47:348–350

0008-4182/11/$-see front matter © 2012 Canadian Ophthalmological Society.Published by Elsevier Inc. All rights reserved.

dx.doi.org/10.1016/j.jcjo.2012.03.039

348   CAN J OPHTHALMOL—VOL. 47, NO. 4, AUGUST 2012

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METHODS

 We recruited, from a pediatric ophthalmology practice,19 subjects with strabismic amblyopia whose visual acu-ities were between 20/300 and 20/40 in their affected eyes.Strabismic amblyopia was defined as reduced vision in 1

eye that had no identified cause other than ocular misalign-ment. The subjects’ nonamblyopic eyes served as the con-trol group. The youngest subject was 9 years old and theoldest was 74 years old. Patients with organic lesions ormedia opacities in either eye, neurologic diseases, ocular orneurologic pathologies affecting the vision of the nonam-blyopic eye, or attention deficit disorders were not eligiblefor the study.

Best-corrected Snellen visual acuity in both eyes was firstassessed without any filters, then with a 0.4 NDF, andfinally with a 3.0 NDF. Kodak (Rochester, NY) WrattenNo. 96 gelatin filter (the same make and strength [3.0NDF] as used in the original 1959 study). An NDF de-creases transmission of light (luminance) through itequally at all wavelengths, without affecting color percep-tion. The optical density of a filter is quantified in log units, which indicate how much light is transmittedthrough the filter (transmission 10OD

100). Thus, a 0.4 NDF has a light transmittance of about 40%, while a 3.0 NDF has a 0.1% light transmittance.

Study subjects were allowed 2 minutes initially to adaptto the reduced illumination of the darkened room. In ad-dition, as per the protocol for the Neutral Density FilterTest outlined in von Noorden’s  Atlas of Strabismus , theNDF was held for 1 minute in front of each eye before

visual acuity was determined.2 Two different Snellencharts were used with each subject to avoid memorizationbias. Visual acuity was converted to logMAR scores andrecorded as the primary outcome. For the second part of the study, visual fields were assessed in both eyes using a Humphrey field analyzer (Carl Zeiss Meditec, Jena, Ger-many), perimeter (visual field assessment 24-2), first with-out any filter then, following a 5-minute break, with a 0.4NDF. Here the mean defect was recorded as the primary outcome.

The data were analyzed to answer 2 questions: (i ) Is therea significant difference in the effect of an NDF on visual acuity 

in nonamblyopic eyesversus eyeswithstrabismic amblyopia?;and(ii ) Is therea significant difference in the effect of an NDFon the mean defect of visual fields in nonamblyopic eyesversus eyes with strabismic amblyopia?

Statistical analysis was conducted using SAS software(SAS Institute, Cary, NC) using the mixed models proce-

dure, assuming compound symmetry structure in the co-variance matrix. This approach is similar to a repeatedmeasures regression but with the advantage of allowing forpairwise comparisons at the same time. A  p  value of lessthan 0.05 was considered statistically significant.

 All data were reviewed by 2 board-certified ophthalmol-ogists and a statistician. The Queen’s University HealthSciences and Affiliated Teaching Hospitals Research Eth-ics Board approved the study for ethical compliance.

RESULTS

 A repeated measures ANOVA test showed that the in-teraction effect between the NDFs and eyes with strabis-mic amblyopia versus the NDFs and nonamblyopic eyes was significantly different ( p     0.0001). There was nosignificant change in visual acuity of nonamblyopic eyesusing a 0.4 NDF versus unfiltered conditions ( p   0.3570), but a significant decrease in visual acuity of nonamblyopic eyes was noted when comparing a 3.0 NDF with unfiltered conditions ( p 0.0001).

There was also a significant improvement in the visualacuity of eyes with strabismic amblyopia when comparing 

a 0.4 NDF to unfiltered conditions ( p

0.0011), but a significant decrease in the visual acuity of eyes with strabis-mic amblyopia when comparing a 3.0 filter to unfilteredconditions ( p 0.0001). The study thus confirmed thateyes with strabismic amblyopia and nonamblyopic eyes areaffected differently by NDF filters when measured by cen-tral visual acuity. Figure 1 and  Table 1 summarize theseresults.

 A repeated measures ANOVA test showed that there was no significant effect on the mean defect of visual fieldsof either amblyopic or nonamblyopic eyes when compar-ing a 0.4 NDF to unfiltered conditions ( p 0.7409).

0

0.2

0.4

0.6

0.8

1

1.2

No Filter NDF 0.4 NDF 3.0

Fellow eyes

Amblyopic eyes

Fig. 1—Comparing least squares means of amblyopic and fellow nonamblyopic eyes with and without neutral density filters (NDF).

 An increase in logMAR represents a decrease in visual acuity.

Effect of neutral density filters on testing— Habeeb et al.

CAN J OPHTHALMOL—VOL. 47, NO. 4, AUGUST 2012   349

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DISCUSSION

The original study by von Noorden and Burian showedan improvement in visual acuity of eyes with strabismicamblyopia when using a 3.0 NDF. In contrast, none of thesubjects in the present study reported any improvement invisual acuity of the eye with strabismic amblyopia whenusing a 3.0 NDF. In fact, using a 3.0 NDF resulted in a significant decrease in visual acuity of nonamblyopic eyesas well as amblyopic eyes ( p    0.0001). One can only speculate that we were unable to replicate the results of the1959 study because of an undisclosed variation in experi-mental protocol or materials used by von Noorden andBurian. However, note there was a larger decrease in visualacuity in nonamblyopic eyes with a 3.0 NDF than in am-blyopic eyes with a 3.0 NDF.

In the Atlas of Strabismus , von Noorden suggests using a 0.5 NDF or a 2.0 NDF to distinguish between strabismicand organic amblyopic.2 It may be that these optical den-

sities are more amenable to obtaining improvements invisual acuity of amblyopic eyes than is a 3.0 NDF. Differ-ences in optical densities notwithstanding, statistical analysisshowed that the interaction effect between NDFs and eyes with strabismic amblyopia versus NDFs and nonamblyopiceyes was significantly different. Moreover, a significant im-provement in visual acuity of amblyopic eyes ( p 0.05) wasnoted when using a 0.4 NDF. This finding is consistent withseveral studies, which show a decrease in luminance may  im-prove visual acuity of eyes with strabismic amblyopia.3-7

The function of the amblyopic eye closely resemblesthat of a nonamblyopic eye under mesopic conditions, be-

cause of the reduced role of cones due to central suppres-sion.3 Eyes with strabismic amblyopia have also beenshown to have improved fixa tion patterns under condi-tions of reduced illumination.3,8 In addition, monocularvision through the amblyopic eye results in improved vi-sual acuity, given that stimulation of the nonamblyopic eyedecreases visual acuity in the amblyopic eye.9  A combina-tion of these 3 factors may thus contribute to the observedimprovement in visual acuity of eyes with strabismic am-blyopia when using an NDF.

 We did not find any significant effect by NDFs on visualfields, as quantified by the mean defect, in eyes with stra-

bismic amblyopia. Our results are consistent with the

study by Mansouri et al., which demonstrated that al-though the maps of the central visual fields in amblyopicsubjects are affected, this finding does not correlate withmeasured visual acuity.10 Thomas showed that contrast sen-sitivityfunctionsobtainedfromthefoveal region of strabismicamblyopes resembled those obtained from the peripheral ret-ina of a nonamblyopic eye.11 Since the 24-2 mean defectmeasures peripheral retinal function more than central retinalfunction, it is not surprising that no difference was found inthe effect of an NDF on mean defect.

In summary, the present study confirms von Noordenand Burian’s observation that neutral density filters affecteyes with strabismic amblyopia differently than they dofellow nonamblyopic eyes. A significant improvement invisual acuity of eyes with strabismic amblyopia was ob-served when using a 0.4 NDF compared to nonamblyopiceyes. In contrast to the 1959 study by von Noorden andBurian, visual acuity was significantly decreased in nonam-blyopic eyes, as well as in eyes with strabismic amblyopia, when viewing through a 3.0 NDF. No significant changein visual fields was observed when using a 0.4 NDF innonamblyopic or amblyopic eyes. Future studies shouldfocus on determining contrast sensitivities using NDFs of multiple optical densities under varied spatial frequencies.This would help determine thresholds, if any, at whicheyes with strabismic amblyopia begin to and cease to re-spond to NDFs of varying intensities. Results can then beanalyzed to determine the ideal NDF resulting in optimalimprovement of visual acuity.

Disclosure: The authors have no proprietary or commercial interestin any materials discussed in this article.

REFERENCES

1. Von Noorden GK, Burian HM. Visual acuity in normal and amblyopicpatients under reduced illumination. I. Behavior of visual acuity withand without neutral density filter. Arch Ophthalmol. 1959;61:533-5.

2. Von Noorden GK. Atlas of Strabismus , 4th ed. St. Louis:  CV Mosby,1983.

3. Von Noorden GK, Burian HM. Visual acuity in normal and amblyopicpatients under reduced illumination. II. The visual acuity at variouslevels of illumination. Arch Ophthalmol. 1959;62:396-9.

4. Lawill T, BurianHM. Luminance, contrast function andvisual acuityinfunctional amblyopia. Am J Ophth. 1966;62:511-20.

5. Sloan LL. Variations in acuity with luminance in ocular disease andanomalies. Doc Ophthalmol. 1969;26:384-93.

6. Hess RF, Howell ER. The luminance-dependent nature of the visualabnormality in strabismic amblyopia. Vision Res. 1978;18:931-6.

7. Hess RF, Campbell FW, Zimmern R. Differences in the neural basis of human amblyopias: The effect of mean luminance.  Vision Res. 1980;20:295-305.

8. Von Noorden GK, Burian HM. An Electro-ophthalmographic study of thebehavior of thefixation of amblyopic eyes in light-and dark-adaptedstate: A preliminary report. Am. J. Ophthalmol. 1958;46:68-77.

9. Von Noorden GK, Leffler MB. Visual acuity in strabismic amblyopia under monocular and binocular conditions.  Arch Ophthalmol.  1966;76:172-7.

10. Mansouri B, Hansen BC, Hess RF. Disrupted retinotopic maps in am-blyopia. Invest Ophthalmol Vis Sci. 2009;50:3218-25.

11. Thomas J. Normal and amblyopic contrast sensitivity functions in cen-

tral and peripheral retinas. Invest Ophthalmol Vis Sci. 1978;17:746-53.

Table 1—Pairwise comparisons of least square means for filtereffects broken down by amblyopic and fellownonamblyopic eyes (n 19)

Pairwise Comparisons Change in Mean

logMAR

Effect

on VA

p  Value

Fellow nonamblyopic eyes

Unfiltered vs 0.4 NDF   0.0302   2   0.3570

Unfiltered vs 3.0 NDF   0.6134   2   0.0001

Amblyopic eyesUnfiltered vs 0.4 NDF   0.1110   1   0.0011

Unfiltered vs 3.0 NDF   0.2345   2   0.0001

NDF, neutral density filter; VA, visual acuity.

Effect of neutral density filters on testing— Habeeb et al.

350   CAN J OPHTHALMOL—VOL. 47, NO. 4, AUGUST 2012