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Identifying Glaucomatous Vision Loss with Visual-Function–Specific Identifying Glaucomatous Vision Loss with Visual-Function–Specific Perimetry in the Diagnostic Innovations in Glaucoma Study Pamela A. Sample, Felipe A. Medeiros, Lyne Racette, John P. Pascual, Catherine Boden, Linda M. Zangwill, Christopher Bowd, and Robert N. Weinreb PURPOSE. To compare the diagnostic results of four perimetric rameters at suggested criterion values provided good sensitiv- tests and to identify useful parameters from each for determin- ity and specificity. FDT showed the highest sensitivity overall, ing abnormality. with SAP performing better than in prior reports. Of note, the METHODS. One hundred eleven eyes with glaucomatous optic same area of the retina was identified as damaged in all tests. neuropathy (GON), 31 with progressive optic neuropathy (Invest Ophthalmol Vis Sci. 2006;47:3381–3389) DOI: (PGON) 53 with ocular hypertension, and 51 with no disease 10.1167/iovs.05-1546 were included (N ϭ 246). Visual field results were not used to classify the eyes. Short-wavelength automated perimetry ver the past several years, psychophysical tests of specific (SWAP), frequency-doubling technology perimetry (FDT), Ovisual functions have been used to measure visual perfor- high-pass resolution perimetry (HPRP), and standard auto- mance and to understand the underlying glaucomatous mated perimetry (SAP) were performed. Receiver operating changes in retinal ganglion cell function. Testing vision with characteristic (ROC) curves were used to compute the areas standard automated perimetry (SAP) is not selective for a par- under the curves (AUC) and sensitivity levels at given specific- ticular ganglion cell type. Any of the primary ganglion cell ities for a variety of abnormality criteria. The agreement among subtypes can respond to an achromatic incremental stimulus tests for abnormality, location, and extent of visual field deficit presented on an achromatic background. In contrast, each were assessed. visual-function–specific perimetric test attempts to isolate a RESULTS. AUC analysis: When the normal group was compared subpopulation of ganglion cells by evaluating a specific visual with the GON group, the FDT pattern SD (PSD) area was larger function characteristically processed by that cell subtype. As than the HPRP PSD (P ϭ 0.020), and the FDT area of total an example, short-wavelength automated perimetry (SWAP) deviation (TD) Ͻ5% was larger than the HPRP mean deviation elicits detection by the short-wavelength cones. The stimulus (MD; P ϭ 0.004). When the normal group was compared with information is then processed through the blue–yellow gan- the PGON group, the FDT area of pattern deviation (PD) Ͻ5% glion cells. The amount of isolation is unknown for each of was larger than the SWAP PSD (P ϭ 0.020). A difference from these function-specific tests, with the exception of SWAP, previous work was that AUCs for PSD or the best SAP were not which provides approximately 15 dB of isolation. This means significantly poorer than those in the function-specific tests. At the blue–yellow ganglion cell system would have to lose 15 dB set specificities, FDT yielded higher sensitivities than all other of sensitivity before another cell type could assist in respond- 1 tests for all parameters. The agreement among tests for abnor- ing to the SWAP stimulus. mality was fair to moderate (␬ ϭ 247–0.563). When loss was Initially, it was hypothesized that the blue–yellow ganglion 2,3 present on more than one test, the quadrant of the visual field cells tested by SWAP were parvocellular. It was later learned 4 5,6 affected was the same in 95% (79/83) of eyes. The number of from Dacey and others that the blue–yellow cells are small eyes identified and number of abnormal quadrants increased bistratified ganglion cells that project their axons to the konio- across groups with increasing certainty of glaucoma. cellular (interlaminar) layers of the lateral geniculate nucleus (LGN) of the thalamus, rather than to the parvocellular layers.7 CONCLUSIONS. At equal specificity, no single perimetric test was Frequency-doubling technology perimetry (FDT)8,9 and vari- always affected, whereas others remained normal. Several pa- ous forms of motion perimetry10–14 attempt to target the magnocellular (also known as parasol) ganglion cells that project to the magnocellular layers of LGN, and high-pass From the Visual Function Laboratory and Hamilton Glaucoma resolution perimetry (HPRP)15,16 is thought to assess the par- Center, Department of Ophthalmology, University of California at San vocellular (also known as midget) ganglion cells that project to Diego, La Jolla, California. the parvocellular layers of LGN. Recent reviews detail the Supported by National Eye Institute Grants EY 08208 (PAS) and evidence supporting anatomic and functional segregation of EY11008 (LMZ) and participant retention incentive grants in the form three primary pathways (parvocellular, magnocellular, and ko- of glaucoma medication at no cost: Alcon Laboratories Inc, Allergan, 17,18 Pfizer Inc, and SANTEN Inc. niocellular) through the LGN. Anatomic projections to Submitted for publication December 5, 2005; revised March 17 cortex and functional preferences within cortical layers are 18,19 and April 10, 2006; accepted June 9, 2006. much less segregated. In addition, the relationship of vi- Disclosure: P.A. Sample, Carl Zeiss Meditec, Inc., Welch-Allyn, sual function to underlying visual pathways is based primarily and Haag-Streit (F); F.A. Medeiros, Carl Zeiss Meditec, Inc. (F); L. on electrophysiology in healthy primates and on lesion stud- Racette, None; J.P. Pascual, None; C. Boden, None; L.M. Zangwill, ies,17 and so some caveats apply in the application of visual- Carl Zeiss Meditec, Inc. (F, R); C. Bowd, None; R.N. Weinreb, Carl function–specific perimetry to ganglion cell assessment (see Zeiss Meditec, Inc. (F, R) the Discussion section). The publication costs of this article were defrayed in part by page charge payment. This article must therefore be marked “advertise- Several studies comparing one visual-function–specific test ment” in accordance with 18 U.S.C. §1734 solely to indicate this fact. to SAP have shown that function-specific tests are superior to Corresponding author: Pamela A. Sample, Department of Ophthal- SAP for early detection of vision loss associated with glau- 20–23 mology, University of California at San Diego, 9500 Gilman Drive, La coma. There are some problems with these studies (see Jolla, CA 92093-0946; [email protected]. the Discussion section). Very few have compared more than Investigative Ophthalmology & Visual Science, August 2006, Vol. 47, No. 8 Copyright © Association for Research in Vision and Ophthalmology 3381 Downloaded from iovs.arvojournals.org on 01/31/2019 3382 Sample et al. IOVS, August 2006, Vol. 47, No. 8 one visual-function–specific test in the same patient popula- Participants. Two hundred forty-six eyes from 246 participants tion.24–26 We first made such a comparison 6 years ago and were evaluated on all three visual-function–specific perimetry tests as evaluated SAP, SWAP, motion automated perimetry (MAP), and well as on SAP. Criteria for classification are detailed later. FDT in 71 eyes with glaucomatous optic neuropathy, 37 ocular Diagnostic categories were based on simultaneous stereoscopic hypertensive eyes, and 28 age-matched normal control eyes.24 color photographs (TRC-SS camera; Topcon America Corp., Paramus, For detection of functional loss, it was found that (1) stan- NJ), obtained after maximal pupil dilation. All photograph evaluations dard visual field testing was not optimal, missing 54% of eyes were taken using a stereoscopic viewer (Stereo Viewer II; Asahi Pen- with glaucomatous optic neuropathy (GON); (2) a combina- tax, Golden, CO) illuminated with color-corrected fluorescent lighting. tion of two or more tests improved detection of functional loss; Two trained and masked graders from the UCSD Optic Disc Reading (3) in an individual, the same retinal location was damaged, Center assessed each photograph independently. Inconsistencies be- regardless of the visual function tested; and (4) SWAP, MAP, tween the two graders’ evaluations were resolved by consensus or and FDT showed promise as early indicators of function loss in through adjudication by a third evaluator. GON was identified by glaucoma. evidence of any of the following: excavation, neuroretinal rim thinning One limitation of this previous study was that the normal or notching, nerve fiber layer defects, or asymmetry of the vertical eyes had normal SAP visual fields and we had to adjust speci- cup-to-disc ratio Ն0.2 between the two eyes. ficities based on other published reports. This limitation does To identify progressive glaucomatous optic neuropathy, two not exist in the present study. A second limitation was the trained graders independently compared the first and last photographs testing of only the koniocellular and magnocellular pathways in each participant’s series. Graders were masked to all other partici- and the lack of a function-specific test preferred by the parvo- pant information, photograph date and test results. Photographs were cellular pathway. We have since obtained sufficient data with graded A equal to B, A worse than B, or A better than B. Inconsistencies HPRP, and in this current study, we to compared it to SWAP, between the two graders’ evaluations were resolved through adjudi- FDT, and SAP in the same individuals. cation by a third evaluator for each pair of photographs. After consen- sus was reached, the temporal sequence of the photographs was unmasked. Progression was defined based on evidence of increasing METHODS excavation, rim thinning or enlarging of notches or nerve fiber layer defects in the later photograph. Changes in rim color and the presence All participants were selected from the ongoing longitudinal Diagnos- of disc hemorrhage or progressive parapapillary atrophy were not tic Innovations in Glaucoma Study (DIGS), conducted at the Hamilton sufficient for characterization of progression. The time frame for pro- Glaucoma Center at the University of California at San Diego (UCSD).
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