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Fixation Stability During Perimetry in Patients with Glaucoma and Split Fixation

E. Lauren Doss MS; Linden Doss MS; R. Philip Doss MD, FACS; Fei Yu PhD; Anne Coleman MD, PhD ABSTRACT. Purpose: Even though a variety of functional tests are used to assess and follow visual loss in glaucoma, standard automated perimetry (SAP) remains the most widely used method. Fixation stability is important for the accuracy of SAP techniques which rely on the assumption that foveal fixation is maintained. We attempt to determine the fixation stability during microperimetry in eyes with glaucomatous scotomas splitting fixation but with residual foveal central vision. Methods: X eyes of X adult subjects with glaucoma were evaluated with confocal scanning laser opthalmoscopy-microperimeter (SLO-MP; Opko/OTI, Toronto, Canada). All eyes had split fixation and visual acuity (VA) of 20/30 or better. Eyes with retinal diseases were excluded. Patient fixation was evaluated during microperimetry with real-time tracking of the eye through registration of the blood vessels and automatic compensation for movement. Scatter plots of fixation positions were generated and bivariate contour ellipse area (BCEA) values were calculated from raw fixation data. A smaller BCEA represents more precise fixation whereas a larger BCEA represents less stable fixation. Results: In our patients (n=Xeyes), the BCEA, the elliptical area containing the eyes fixation position 68% of the time, ranged from 391.4 minarc2 to 11368 minarc2, compared to a range of 100 min to 650 minarc2 in normal populations described elsewhere. Five patients had normal BCEA (mean 40284.4 minarc2), 4 had intermediate (mean 1565490 minarc2), and 6 had markedly abnormal (mean 9,1322890 minarc2). Of our X patients, X had eccentric BCEA and X had central BCEA. Interestingly, we found no correlation between centricity of the BCEA and fixation stability. Conclusions: The computerized fixation control when performing microperimetry with the SLO-MP allows precise determination of fixation stability in glaucoma patients. Our results suggest that fixation stability is compromised in some patients with advanced glaucoma even when the VA is foveal (20/30 or better). In these patients, fixation is not always foveal, nevertheless the SAP will still be mapped as though fixation were in the center of the field, and tested points will be shifted relative to their true retinal locations. Keywords: Glaucoma, Perimetry, Fixation. INTRODUCTION. When the eye fixates upon a point,there is some retinal motion due to involuntary eye movements such as physiological nystagmus,drifts and microsaccades as well as correcting movements to compensate for motion of the head (Steinman et al.,1982; Carpenter, 1988). In those without eye disease,the locus of fixation will lie within the foveola. Fixation stability, the ability to focus the retina on an image, is critical to reading and safe performance of activities of daily living (Crabb et al, 2010). It has been studied, particularly in the context of macular disease using the technology of confocal scanning laser opthalmoscopy (SLO) and microperimetry (MP)(Crossland et al, 2009; Kosnik et al., 1986; Tarita-Nistor et al., 2009; Rohrschneider et al., 1995).

SLO-MP OCT, which combines these technologies, relies on electronic tracking of the retinal vasculature, allowing precise measurement of fixation stability. While it is not a new concept to the field of retina, fixation stability remains relatively unexplored as it relates to glaucoma. This is despite its importance to the pillar of glaucoma management, standard automated perimetry (SAP) techniques, which rely on the assumption that foveal fixation is maintained. Indeed, if fixation is eccentric or unstable, the results of SAP will be compromised by being mapped as though fixation were in the center of the field, and tested points will be shifted relative to their true retinal locations. The ability to hold the eye steady while observing a target, called fixation stability, is crucial to day-today precision tasks including reading and driving. It is commonly known that fixation stability is compromised in retinal disease; yet although it is an important concept to the accuracy of many glaucoma tests, it has hardly been studied in patients with glaucoma. Steady fixation is generally associated with good central vision. However, in our preliminary study, about half of our subjects had poor fixation stability despite good central vision (i.e. Vision sufficient to drive and read). For these glaucoma patients, traditional glaucoma tests that rely on steady fixation yield inaccurate results that may bias their treatment. Validating these results is important to improving glaucoma management and will enhance our understanding of the glaucoma patients ability to safely perform essential functions such as driving. METHODS. In this prospective, non-randomized cohort study, fifty eyes of fifty adult subjects with glaucoma and twenty eyes of twenty adult subjects without glaucoma will be evaluated with confocal scanning laser opthalmoscope-microperimetry (SLO-MP; Opko/OTI, Toronto, Canada). Patients were recruited during the routine office visit, and informed consent for participation in the study was obtained. The UCLA Human Subjects Review Board and I&E Reviews approved this study. All eyes were selected for split fixation and visual acuity (VA) of 20/30 or better. Eyes with retinal diseases were excluded. Patient fixation was evaluated during microperimetry with real-time tracking of the eye through registration of the blood vessels and automatic compensation for movement. Scatter plots of fixation positions were generated. Raw data was extracted from the softwares output using Adobe Illustrator to determine the coordinates. From this scatter plot of raw fixation data, the bivariate contour ellipse area (BCEA) values were calculated using a P value of 68% (k = 1.14) as previously described (Crossland et al., 2002 and 2009). A smaller BCEA represents more precise fixation whereas a larger BCEA represents less stable fixation. The weighted distance from the origin determines centricity. The means, standard deviations, and confidence intervals for BCEA and centricity were determined. The relationship between BCEA size and centricity were analyzed statistically. RESULTS. We found the bivariate contour ellipse area (BCEA), the elliptical area containing the eyes fixation position 68% of the time, ranged from 391.4 minarc2 to 11368 minarc2, compared to a range of 100 minarc2 to 650 minarc2 in normal populations described elsewhere (Crossland et al., 2002). Five patients had normal BCEA (mean 40284.4 minarc2), 4 had intermediate (mean 1565490 minarc2), and 6 had markedly abnormal (mean 9,1322890 minarc2). Of our 15 patients, 11 had eccentric BCEA

and 4 had central BCEA. Interestingly, we found no correlation between centricity of the BCEA and fixation stability (p=0.01). DISCUSSION. Our study indicates that fixation stability is severely compromised in a third of patients even when visual acuity is foveal. In these patients with excellent central vision, fixation is unexpectedly extrafoveal, nevertheless standard perimetry will still be mapped as though fixation were in the center of the field causing tested points to appear shifted relative to their true retinal locations.

Even though a variety of functional tests are used to assess and follow visual loss in glaucoma, standard automated perimetry (SAP) remains the most widely used method. Fixation stability is important for the accuracy of SAP techniques, which rely on the assumption that foveal fixation is maintained. We characterize and quantify the fixation stability during microperimetry in eyes with glaucomatous scotomas splitting fixation but with residual foveal central vision (visual acuity 20/30). We hypothesize based on our results that patients with advanced glaucoma who have reasonably preserved visual acuity may still demonstrate poor fixation. In addition, we intend to confirm or reject the hypothesis that centricity of fixation predicts better fixation stability in these patients. The SLO has been used in the study of glaucoma (Weinreb et al., 2010). Recently the correlation between macular sensitivity using SLO-MP with the paracentral visual field as determined by SAP has been confirmed (Lima et al., 2009). However, aside from this validation of the combined technology, we present the first study using it in glaucoma and the first using it to investigate fixation stability. Fletcher and colleagues devised a PRL scoring system based on fixation stability,pursuit ability and saccade to PRL ability (Fletcher et al.,1993; Schuchard and Fletcher,1994). They found that this score was superior to visual acuity in predicting reading speed and accuracy in patients with central scotomas. It is perhaps surprising that there is no relationship between scotoma size and fixation stability,as fixation is known to be less precise as eccentricity increases(Sansbury et al.,1973),and a larger scotoma will lead to a more eccentric PRL being used. However,this lack of correlation has been reported previously (Timberlake et al.,1986; White and Bedell, 1990).
The ability to obtain more accurate visual fields will go a long way toward improving the management of glaucoma. One of the major drawbacks of SAP is the reliance on patient cooperation, which may often deteriorate with increasing eye strain and fatigue (Heijl and Asman, 1995). Stamina is a particularly pronounced factor during the longer threshold tests, evidenced by an increase in fixation errors that may invalidate the test reliability and necessitate repeat testing. The usefulness of electronic tracking technology, as is used in the SLO-MP, in not only eliminating these practical complications but also increasing the accuracy of the results by measuring and adjusting for fixation instability will be a tremendous advance in glaucoma management and patient comfort. Considering this, it is not inconceivable that tracking-modulated SAP may soon replace fixation-dependent SAP in glaucoma management.

We believe that these eyes are employing a compensatory saccadic activity in an attempt to brush over the deficits of neighboring visual field.

REFERENCES: Crabb DP, Smith ND, Rauscher FG, Chisholm CM, Barbur JL, et al. (2010) Exploring Eye Movements in Patients with Glaucoma When Viewing a Driving Scene. PLoS ONE 5(3): e9710. Crossland MD, Rubin GS. The Use of an Infrared Eyetracker to Measure Fixation Stability. Optom Vis Sci 2002;79:735739 Crossland MD, Dunbar HM, Rubin GS. microperimeter.Retina. 2009 May;29(5):651-6. Fixation stability measurement using the MP1

Lima VC, Prata TS, De Moraes CGV, Kim J, Seiple W, Rosen RB, Liebmann JM, Ritc R. A comparison between microperimetry and standard achromatic perimetry of the central visual field in eyes with glaucomatous paracentral visual-field defects. Br J Ophthalmol 2010;94:6467. Rohrschneider K, Becker M, Kruse FE, Fendrich T, Volcker HE. Stability of fixation: results of funduscontrolled examination using the scanning laser ophthalmoscope. Ger J Ophthalmol 1995; 4: 197-202. Schuchard RA, Fletcher DC. Preferred retinal locus: a review with applications in low vision rehabilitation. Ophthalmol Clin North Am 1994; 7: 243-56. Tarita-Nistor L, Gonzalez EG, Mandelcorn MS, Lillakas L, Steinbach MJ. Fixation Stability, Fixation Location, and Visual Acuity after Successful Macular Hole Surgery. Invest Ophthalmol & Vis Sci. Jan 2009;50:1. Timberlake GT, Mainster MA, Peli E, Augliere RA, Essock EA, Arend LE. Reading with a macular scotoma: I. Retinal location of scotoma and fixation area. Invest Ophthalmol Vis Sci 1986; 27: 1137-47. William Kosnik,* John Fikre,* and Robert Sekulerf. Visual Fixation Stability in Older Adults. Invest Ophthalmol Vis Sci 27:1720-1725, 1986. Weinreb RN, Zangwill LM, Jain S, Becerra LM, Dirkes K, Piltz-Seymour JR, Cioffi GA, Trick GL, Coleman AL, Brandt JD, Liebmann JM, Gordon MO, Kass MA; OHTS CSLO Ancillary Study Group. Predicting the onset of glaucoma: the confocal scanning laser ophthalmoscopy ancillary study to the Ocular Hypertension Treatment Study. Ophthalmology. 2010 Sep;117(9):1674-83. Heijl A, Asman P. Pitfalls of automated perimetry in glaucoma diagnosis. Curr Opin Ophthalmol. 1995 Apr;6(2):46-51.

TRASH
Purpose: Fixation stability is important to standard perimetry accuracy. Methods: To study a relationship between foveal vision and fixation stability in advanced glaucoma, we evaluated 27 eyes (23 subjects) with glaucomatous scotomas splitting fixation but maintained central vision (visual acuity;VA 20/30) by confocal scanning laser opthalmoscope-microperimetry. Bivariate contour ellipse areas (BCEA) were calculated to include 68% of fixation points. Results: 17 eyes (mean 355.3170.8 minarc2) fell within a normal range compared to others normative data (p=0.002). Mean abnormal was 1416.1728.6 minarc2. Visual field scores correlated with BCEA (R=-0.39; p=0.042). Conclusion: Fixation stability is severely compromised in some patients with advanced glaucoma despite foveal VA. Precis: Analysis of results from microperimetry with electronic tracking suggests that fixation stability is severely compromised in some patients with advanced glaucoma despite preserved central visual acuity. In these patients, fixation is not always foveal, nevertheless standard perimetry will still be mapped as though fixation were in the center of the field, and tested points will be shifted relative to their true retinal locations. Abstract: Purpose: Fixation stability is important to standard perimetry accuracy. Methods: To study a relationship between foveal vision and fixation stability in advanced glaucoma, we evaluated 27 eyes (23 subjects) with glaucomatous scotomas splitting fixation but maintained central vision (visual acuity;VA 20/30) by confocal scanning laser opthalmoscopemicroperimetry. Bivariate contour ellipse areas (BCEA) were calculated to include 68% of fixation points. Results: 17 eyes (mean 355.3170.8 minarc2) fell within a normal range compared to others normative data (p=0.002). Mean abnormal was 1416.1728.6 minarc2. Visual field scores correlated with BCEA (R=-0.39; p=0.042). Conclusion: Fixation stability is severely compromised in some patients with advanced glaucoma despite foveal VA. OLD ABSTRACT:

BACKGROUND. Fixation stability, the ability to hold the eye steady when observing a point target, is a critical function of the fovea, and often studied in retinal disease. Conventional perimetry assumes stable foveal fixation, which is can be a false assumption in patients with macular scotoma who often use an eccentric retinal location for fixation, which is often less stable than foveal fixation.Thus, conventional perimetry, falsely assuming foveal fixation, will show an eccentric displacement of the macular scotoma in such patients (Markowitz &Muller, 2004). As a result, macular scotometry based on conventional perimetry often has limited accuracy due to unstable eccentric fixation.

PURPOSE. The aim of our study is to describe the fixation instability or microdeviations in fixation present in advanced glaucomatous patients. We utilized the tracking capacity of the the scanning laser ophthalmoscopemicroperimeter (SLO-MP, Opko) to follow the fixation patterns in these patients. BACKGROUND METHODS. The following are descriptions of what we are trying to do from some similar studies in patients with Retinal disease. Fixation stability was denned by the scatter of eye positions about their mean position. This measure was described by the two-dimensional area of the bivariate contour ellipse expressed in minutes of arc squared.17 To determine if the fixation of older observers was less steady than that of young observers, we analyzed two measures of fixation stability: 1) the bivariate con- tour ellipse area (BA), and 2) the standard deviation of the eye positions along the horizontal and vertical meridia. The second measure was used because, as re- ported earlier, horizontal and vertical eye movements may be differentially affected by aging.9'10
Leigh RJ: The impoverishment of ocular motility in the elderly. In Aging and Human Visual Function, Sekuler R, Kline D, and Dismukes K, editors. New York, Alan R Liss, 1982, pp. 173-180.

The spatial distribution of these fixation points can be measured and related to fixation stability: a subject with a small area of fixation will have more stable fixation than one with a larger area. Fixation stability is impaired in patients with macular disease, 3-6and this may be one reason for their reduced visual performance. In recent years, the scanning laser ophthalmoscope (SLO) has become the instrument of choice in the measurement of the retinal area used for fixation. 6-8
3. Rohrschneider K, Becker M, Kruse FE, Fendrich T, Volcker HE. Stability of fixation: results of fundus-controlled examination using the scanning laser ophthalmoscope. Ger J Ophthalmol 1995; 4: 197-202. Cited Here... | PubMed 4. Schuchard RA, Fletcher DC. Preferred retinal locus: a review with applications in low vision rehabilitation. Ophthalmol Clin North Am 1994; 7: 243-56. Cited Here... 6. Timberlake GT, Mainster MA, Peli E, Augliere RA, Essock EA, Arend LE. Reading with a macular scotoma: I. Retinal location of scotoma and fixation area. Invest Ophthalmol Vis Sci 1986; 27: 1137-47. Cited Here... | PubMed 7. Culham LE, Fitzke FW, Timberlake GT, Marshall J. Use of scrolled text in a scanning laser ophthalmoscope to assess reading performance at different retinal locations. Ophthalmic Physiol Opt 1992; 12: 281-6. Cited Here... | PubMed | CrossRef 8. Schuchard RA, Raasch TW. Retinal locus for fixation: pericentral fixation targets. Clin Vision Sci 1992; 7: 51120. Cited Here...