Reversal of Optic Disc Cupping after Glaucoma Surgery Analyzed with a Scanning Laser Tomograph Mark R. Lesk, MD, George L. Spaeth, MD, Augusto Azuara–Blanco, MD, Silvana V. Araujo, MD, L. Jay Katz, MD, Annette K. Terebuh, MD, Richard P. Wilson, MD, Marlene R. Moster, MD, Courtland M. Schmidt, MD Objective: To detect and quantitate changes in optic nerve morphology after glaucoma surgery using the Heidelberg Retina Tomograph (HRT, Heidelberg Instruments, Heidelberg, Germany). Design: Nonconsecutive observational case series. Participants and Intervention: The authors prospectively enrolled 21 adult patients undergoing incisional glaucoma surgery for progressive glaucoma damage. Quantitative analysis of the optic nerve head by scanning laser tomography and automated perimetry were performed before and after glaucoma surgery. Main Outcome Measures: Changes in optic nerve parameters were subjected to linear regression analysis with respect to percent of postoperative reduction of intraocular pressure (IOP), as well as with respect to age, refraction, preoperative cup:disc ratio, and change in visual field parameters. Results: Seventeen patients had pre- and postoperative images suitable for analysis. Mean IOP at the time of image acquisition before surgery was 30.5 ⫾ 12 mmHg, and after surgery 11.8 ⫾ 5.2 mmHg (mean follow-up, 26 ⫾ 7 weeks). Eleven of 13 (85%) patients having IOP reduction of greater than 40% showed improvement in optic disc parameters. All four patients with less than 25% reduction in IOP showed worsening of most parameters. Changes in optic disc parameters were highly correlated with percent IOP reduction and with age. The parameters in which change most strongly correlated with percent change of IOP were cup area, rim area, cup:disc ratio, and mean cup depth (each, P ⬍ 0.005). The age of the patient correlated highly with change in maximum cup depth (P ⬍ 0.005). Refraction and clinically determined cup:disc ratio correlated poorly with changes in measured optic disc parameters. Clinical improvement in visual fields was correlated with the degree of improvement of cup:disc ratio (P ⫽ 0.025). Conclusion: Most patients showing a 40% lowering of IOP after glaucoma surgery show improved optic nerve morphology as measured by the HRT. The amount of improvement correlated highly with the percent reduction of IOP. Ophthalmology 1999;106:1013–1018 Regression of optic nerve cupping or improvement of the appearance of the neuroretinal rim are common after successful glaucoma surgery in children but are less commonly observed in adults. Regression of cupping has been proposed as possibly more reliable than attainment of a target
Originally received: April 15, 1998. Revision accepted: December 21, 1998. Manuscript no. 98196. From the William and Anna Goldberg Glaucoma Service and Research Laboratories, Wills Eye Hospital, Jefferson Medical College, Thomas Jefferson University, Philadelphia, Pennsylvania. Mark R. Lesk is currently affiliated with the Maisonneuve-Rosemont Hospital, Montreal, Quebec, Canada. Supported by the Glaucoma Service Foundation to Prevent Blindness, Philadelphia, the Scholler Foundation, Philadelphia, and Merck & Co. Inc., West Point, Pennsylvania. The authors have no proprietary interest in the Heidelberg Retina Tomograph. Address correspondence to George L. Spaeth, MD, Wills Eye Hospital, 900 Walnut St., Philadelphia, PA 19107-5598.
intraocular pressure (IOP) as a predictor for stabilization of glaucomatous optic neuropathy.1 Thirty percent of patients with at least a 30% reduction in IOP after glaucoma therapy had an improvement of optic disc appearance to masked readers of stereo disc photos in one study2; some of the patients in this study also had improvement of visual fields. Using the Rodenstock Optic Nerve Head Analyzer (Rodenstock Instruments, GmbH, Munich, Germany), Shin et al3 observed improvement of optic nerve parameters in 77% of patients having at least a 30% reduction in IOP. Using the same instrument, Funk4 noted improvement in neuroretinal rim area in 10 of 18 eyes after glaucoma surgery. If we were able to detect subtle changes in optic disc morphology, improved appearance of the optic disc could presumably be more carefully evaluated as a predictor of clinical stability. Laser tomographic scanning is a relatively new technique of confocal fundus imaging that allows three-dimensional image reconstruction of the optic nerve head. It appears to be more accurate and reproducible than tech-
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Ophthalmology Volume 106, Number 5, May 1999 niques based on human observers or computerized analysis of stereo optic disc photographs.5–9 The Heidelberg Retina Tomograph (HRT, Heidelberg Instruments, Heidelberg, Germany) has a reproducibility of approximately 30 m10 and coefficients of variation of around 5%.5 We used this technology to search for changes in the optic disc of glaucoma patients after surgical IOP reduction. We also examined changes in optic disc photographs and automated perimetry in these patients.
Methods Twenty-one patients with glaucoma scheduled for a guarded filtration procedure (GFP) or a tube shunt implantation in our referral practices between August 1994 and December 1994 were recruited for HRT imaging and automated perimetry during the month prior to surgery. Five additional patients who were solicited for this study were unwilling or unable to participate. Patients were selected based on their ability to perform perimetry reliably and the clarity of their ocular media. An effort was made as well to have a wide range of preoperative clinically evaluated cup:disc ratios and IOPs within the test group. Patients scheduled for procedures other than GFP or tube shunt implantation were excluded, as were patients having ocular pathology other than glaucoma. Intraocular pressure was measured within 1 hour of the HRT imaging. Pupils smaller than 3 mm were dilated before HRT image acquisition. After HRT images were obtained, undilated pupils were dilated for optic disc photography using the Topcon TRC-SS simultaneous camera (Topcon, Inc., Paramus, NJ) and a 30° split frame field. Automated perimetry was performed preoperatively using the Humphrey Field Analyzer, program 24-2 (Humphrey Instruments, San Leandro, CA) (except for one patient for whom the Octopus, program 31 [Haag-Streit International, Mason, OH], was used). At the time of automated perimetry, pupil size was documented. Postoperative imaging and perimetry were obtained a minimum of 14 weeks after surgery. Images of the optic disc were obtained with the HRT, which works on the principle of confocal scanning. A beam of laser light (670 nm) is focused and illuminates a single spot on a particular focal plane. The HRT produces an image by sequentially scanning the retina with one spot of laser. The field of view scanned can be varied between 10 and 20 degrees. In order to get a three-dimensional image, the focal point of the laser is moved, and the scan is repeated in 32 different planes, covering a range of 0.5 and 4 mm. Each image contains approximately 65,000 picture elements or “pixels.” For each pixel, there is a separate height measurement. The light reflected from each single point is directed to a detector, where it is registered, digitized, and stored by a computer. In this study, single images were obtained using a 10-degree field of view. Heidelberg Retina Tomograph images were analyzed using software version 1.11. The reference plane is located 50 m posterior to the mean height of the temporal peripapillary retina, in the segment between ⫺10 degrees and ⫺4 degrees. The parameters studied are summarized in Table 1. The optic disc boundary (“contour line”) was established on the preoperative image by the operator, using the interactive measure mode, and the boundary was transferred automatically to the postoperative image. Change in disc parameters was calculated and correlated with other variables by calculating the Pearson correlation coefficients or by using linear regression analysis calculating r and r2. Results were analyzed for statistical significance using the Student’s t-test and the F-statistic.
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Table 1. Heidelberg Retina Tomograph Parameters Disc area (mm2): total area within the contour line Cup area (mm2): total area of those parts within the contour located below the reference plane* Cup/disc area ratio: “cup area” divided by “disc area” Rim area (mm2): “Disc area” minus “cup area” Cup volume (mm3): total volume of those parts within the contour line† located below the reference plane Rim volume (mm3): total volume of those parts within the contour line located above the reference plane Height variation contour (mm): difference in height between the highest and lowest points of the contour line Mean RNFL thickness (mm): mean elevation of the retinal surface along the contour line above the reference plane RNFL cross section area (mm2): same as “Mean RNFL thickness” times the length of the contour line Mean cup depth (mm): mean depth of the part inside the contour line Maximum cup depth (mm): mean depth of the 5% picture elements with the highest depth values within the contour line Cup shape measure: description of the overall shape (skewness) of the optic nerve head. Values are typically negative in normal eyes (flat cup) and positive in glaucomatous eyes (high slopes at the cup boundary) * Reference plane: plane located 50 m posteriorly of the mean contour line height in the segment between ⫺10° and ⫺4°. † Contour line: the observer draws a line overlying the optic disc boundary. The height along this contour line is corrected for artifacts due to crossing blood vessels that cause local elevations.
Heidelberg Retina Tomograph parameters were considered improved if they demonstrated decreased cupping or increased neuroretinal rim or retinal nerve fiber layer (RNFL). Pre- and postoperative visual fields were presented paired in random order (to mask which field was preoperative and which was postoperative) to three masked glaucoma subspecialists who independently graded the second field of each pair as “better,” “same,” or “worse” using personal subjective criteria. These criteria included significant changes in localized glaucomatous scotomas in fields having acceptable reliability indices. The same masked grading system was followed for evaluation of pre- and postoperative optic disc photographs.
Results Twenty patients completed the required HRT imaging (one patient was unable to return to the study center for imaging). Of these, 3 patients had poor-quality HRT images that could not be analyzed, and 17 patients (17 eyes) had good-quality HRT images both preand postoperatively. Sixteen of these patients had adequate pairs of visual fields. Ten patients had both pre- and postoperative optic disc photographs that were satisfactory for analysis. Of the 17 patients analyzed, 16 underwent GFP, and one had a single-plate Molteno tube shunt implantation. Patient characteristics are presented in Table 2. The mean age was 55.3 years (standard deviation [SD], ⫾ 13.0 years; range, 33– 80 years). There were 9 women and 8 men; 15 subjects were white and 2 were black. Clinical evaluation of cup:disc ratios indicated nine patients with cup:disc ratios of 0.7 or less and eight with cup:disc ratios of 0.8 or more. Mean refractive error was ⫺1.3 ⫾ 3.0 diopters (D). Three patients had a refractive error between ⫺5 D and ⫺8 D. The mean defect on automated perimetry averaged ⫺7.0 dB (SD, ⫾ 5.9 dB; range, ⫹0.2 to ⫺17.6 dB).
Lesk et al 䡠 Reversal of Cupping Table 2. Patient Characteristics Patient No.
Age (yrs)
Sex
Diagnosis
Preop IOP
% Drop IOP
Change C/D HRT
Change Field
Change Photos
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17
62 68 72 50 60 80 33 35 47 67 57 52 47 57 65 43 45
M F F M M M F M F M M F F F M F F
POAG SOAG NTG PIGM G POAG EXFOL POAG POAG EIA POAG POAG POAG POAG CACG POAG SOAG POAG
19 27 18 18 15 39 27 21 42 28 33 26 24 50 28 58 43
11 15 17 22 47 49 52 52 62 64 64 69 71 78 82 86 91
⫹0.09 ⫹0.01 ⫹0.02 ⫹0.05 ⫺0.16 ⫺0.05 ⫹0.13 0.00 ⫺0.02 ⫺0.33 ⫺0.26 ⫺0.07 ⫺0.07 ⫺0.15 ⫺0.21 ⫺0.23 ⫺0.29
? S B S ? N/A ? S S B B S W B B S B
S N/A S B S N/A N/A N/A N/A W B ? B N/A N/A B B
C/D ⫽ cup area/disc area ratio; HRT ⫽ Heidelberg Retina Tomograph; Field ⫽ subjective evaluation of change of pre- and postoperative perimetry; Photos ⫽ subjective evaluation of change of pre- and postoperative disc photographs; S, B, W ⫽ agreement by at least two of three specialists that disc or field is same, better, or worse; ? ⫽ no agreement; N/A ⫽ not available; POAG ⫽ primary open-angle glaucoma; SOAG ⫽ secondary open-angle glaucoma; NTG ⫽ normal-tension glaucoma; PIGM G ⫽ pigmentary glaucoma; EXFOL ⫽ exfoliative glaucoma; EIA ⫽ essential iris atrophy and glaucoma; CACG ⫽ chronic angle-closure glaucoma.
Images were obtained at mean times of 7 ⫾ 16 days preoperatively and 26 ⫾ 7 weeks postoperatively. One patient was imaged 2 months before surgery (patient 7 in Table 2). Visual fields were obtained less than 3 months prior to surgery. Mean preoperative IOP was 30.5 ⫾ 12 mmHg (range, 15–58 mmHg). Mean postoperative IOP at the time of HRT acquisition was 11.8 ⫾ 5.2 mmHg (range, 4 –23 mmHg). Based on the IOP drop, we divided the patients into two groups: four patients had reductions of IOP ranging from 11% to 22% (group A), and the remainder (n ⫽ 13) had reductions of at least 47% (group B). In each member of group A, all or most of the HRT optic disc parameters worsened. In 11 of 13 (85%) members of group B, all or most of the disc parameters improved. The two patients in group B who did not improve were young myopes who each had a 52% drop in IOP (Table 2, patients 7 and 8). One of these patients had stable parameters, and the other showed worsening.
Linear regression analysis for all 17 patients revealed a strong correlation between the percent decrease in IOP and many of the HRT parameters (Figs 1– 4). Changes in the following parameters were correlated with percent reduction in IOP: cup area:disc area ratio (r ⫽ ⫺0.72; P ⬍ 0.005), cup area (r ⫽ ⫺0.70; P ⬍ 0.005), rim area (r ⫽ 0.69, P ⬍ 0.005), cup volume (r ⫽ ⫺0.59; P ⬍ 0.025), rim volume (r ⫽ 0.59; P ⬍ 0.025), mean cup depth (r ⫽ ⫺0.72; P ⬍ 0.005), and maximum cup depth (r ⫽ ⫺0.57; P ⬍ 0.025). Changes (in most cases increases) in RNFL thickness and RNFL cross-sectional area were also positively correlated with change in IOP (r ⫽ 0.44; P ⫽ 0.08 and r ⫽ 0.43; P ⫽ 0.09, respectively), but this correlation did not reach statistical significance. Changes in the contour of the height of the cup and in measurements of the shape of the cup did not show a significant relationship to change in IOP (r ⫽ ⫺0.22; P ⫽ 0.40 and r ⫽ 0.40; P ⫽ 0.11, respectively).
Figure 1. Relationship between percent drop of IOP after surgery and the change in cup:disc area ratio assessed by the HRT. More substantial reductions in IOP correlated with reduced cup:disc ratios (r ⫽ ⫺0.72; P ⬍ 0.005).
Figure 2. Relationship between percent drop of IOP after surgery and the change in rim area (open squares) and cup area (black squares) assessed by the HRT. More substantial reductions in IOP correlated with reduced cup area (r ⫽ ⫺0.70; P ⬍ 0.005) and increased rim area (r ⫽ 0.69; P ⬍ 0.005).
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Figure 3. Relationship between drop of IOP after surgery and the change in rim volume (open squares) and cup volume (black squares) assessed by the HRT. More substantial reductions in IOP correlated with reduced cup volume (r ⫽ ⫺0.59; P ⬍ 0.025) and increased rim volume (r ⫽ 0.59; P ⬍ 0.025).
For the 13 patients having at least 40% reduction in IOP (group B), changes in the following parameters were positively correlated with progressive age: maximum cup depth (r ⫽ ⫺0.78; P ⬍ 0.005), mean cup depth (r ⫽ ⫺0.63; P ⬍ 0.05; Fig 5) and cup volume (r ⫽ ⫺0.61; P ⬍ 0.05). This correlation was independent of percent reduction of IOP within this group; the older patients (n ⫽ 6; mean age ⫽ 64.3 years) tended to have slightly smaller reductions in IOP than the younger patients (n ⫽ 7; mean age ⫽ 43.1 years) (64% vs. 69% reduction of IOP; P ⫽ not significant). For group B, refraction correlated with change in cup shape only (r ⫽ ⫺0.61; P ⬍ 0.05), with more myopic eyes having a greater reduction in this parameter postoperatively. Clinically evaluated preoperative cup:disc ratio did not correlate with changes in any of the parameters for either group or for the whole population. Both pre- and postoperative visual fields were available for 16 patients. Visual fields were considered to have improved by at least 2 of the 3 readers in 1 of 3 patients in group A (33%) and in 5 of 13 patients in group B (38%, P ⫽ not significant). Patients having visual fields judged to be improved (n ⫽ 6) had mean improve-
Figure 5. Relationship between patients’ age and the change in mean cup depth (open squares) and maximum cup depth (black squares) assessed by the HRT. Greater age correlated with reduced mean cup depth (r ⫽ ⫺0.63; P ⬍ 0.05) and reduced maximum cup depth (r ⫽ ⫺0.78; P ⬍ 0.005).
ment of cup:disc ratio of 0.20 as measured by the HRT, whereas those having fields judged to be the same or worse (n ⫽ 7) had mean cup:disc ratio improvement of 0.05, a difference that was statistically significant (P ⫽ 0.025, t-test). Five of 6 patients (83%) showing at least 0.15 improvement in cup:disc ratio as measured by the HRT were judged to have had field improvement compared with 1 improved field among the remaining 10 patients (10%), a difference that was statistically significant by chi-square analysis (P ⬍ 0.005). Both pre-and postoperative statistical visual field parameters were available for 14 patients. We found no correlation between the change in mean defect (r ⫽⫺0.17; P ⫽ 0.6), pattern standard deviation (r ⫽ 0.17; P ⫽ 0.6), or corrected pattern standard deviation (r ⫽ 0.21; P ⫽ 0.5) and the change in cup:disc ratio as measured by the HRT. Both pre- and postoperative standard optic disc photographs were available for ten patients. In group A, one of three (33%) discs were judged to have improved, whereas in group B four of seven (57%) were considered improved by a majority of readers (P ⫽ not significant). Among the four patients with the greatest improvement of cup:disc ratio as evaluated by the HRT, three were considered to have improved optic disc appearance on standard optic disc photographs.
Discussion
Figure 4. Relationship between drop of IOP after surgery and the change in mean cup depth (open squares) and maximum cup depth (black squares) assessed by the HRT. More substantial reductions in IOP correlated with reduced mean cup depth (r ⫽ ⫺0.72; P ⬍ 0.005) and reduced maximum cup depth (r ⫽ ⫺0.57; P ⬍ 0.025).
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Using the HRT, we were able to detect improvement in optic disc parameters in 85% of patients having IOP reductions of at least 40% and in 0% of patients having IOP reductions of less than 25%. In linear regression analysis, most changes of the disc parameters correlated highly with percent reduction of IOP; some correlated with the patients’ age. The fact that greater disc parameter improvement was measured in eyes that had greater IOP reduction lends consistency to this data. Those patients having the greatest improvement in cup: disc ratios by HRT analysis were likely to have fields or disc photographs judged improved by our glaucoma specialists. This correlation supports the trend apparent in the HRT
Lesk et al 䡠 Reversal of Cupping data. Similarly, Shin et al3 judged there to be stereophotographic optic disc improvement in 5 of 10 eyes showing improvement of optic disc parameters by the Rodenstock computer analysis. However, they did not evaluate visual fields. Analysis of optic disc topography with the HRT has higher reproducibility than human or computer analysis of stereophotographs.5,6 The confocal imaging used by the HRT also allows improved accuracy in depth perception.5 These factors probably explain why the HRT is able to detect reversal of cupping in a high fraction of patients undergoing substantial IOP reductions. Postoperative imaging was performed after a relatively long delay, averaging 6.2 months, to avoid imaging during a period of possible disc edema. Three of our patients had IOPs of less than 8 mmHg (7, 5.5, and 4 mmHg), and these eyes were imaged 5, 7, and 8 months postoperatively. There was no clinical sign of disc edema or hypotony maculopathy in these or in any other patient in this study. Therefore, it seems highly improbable that postoperative edema accounts for the findings. Reversal of optic disc cupping after IOP lowering was first reported in 186911 and is commonly observed in children. Katz et al2 reviewed stereophotographs and visual fields of patients undergoing glaucoma treatment. Among those patients having at least a 30% reduction in IOP, 30% had improved disc appearance and 40% had improved visual fields. Using computer analysis of optic disc stereophotographs, Shin et al3 detected reversal of all optic disc parameters in 8 of 13 eyes; mean IOP reduction was 48%. Using the same technique, Funk4 detected increased neuroretinal rim area in 44% of his patients undergoing glaucoma surgery. We may have detected a higher rate of improvement of optic disc parameters due to greater sensitivity of the HRT, variations in patient selection, or greater IOP lowering. Although our study was not designed to compare the detection of changes in cupping by the two techniques, our results suggest that the HRT may be more sensitive to changes in cupping than is stereo optic disc photography. Recently, Raitta et al12 used the HRT to study changes in optic disc topography after glaucoma surgery in nine patients. They found a reduction in optic disc cup volume in all but one of the eyes that had at least a 30% IOP reduction. The mean cup depth was reduced significantly for this group after 3.7 months of follow-up. The cup:disc ratio was significantly reduced for a subgroup of patients after 12 months, whereas the mean height of contour (representing the surface height of the RNFL) was increased. However, no significant correlation between IOP changes and the changes in optic disc parameters was noted. The present study revealed similar changes in optic disc parameters but was able to correlate many of them with changes in IOP. Irak et al13 have also examined reversal of cupping after glaucoma surgery using the HRT and also found a good correlation between changes in most optic disc parameters and percent reduction of IOP. They did not look at visual field changes or standard disc photos. They did not examine mean cup depth but found that maximum cup depth was not correlated with percent reduction of IOP. We found that these cup depths both shallowed with IOP reduction. This
may explain part of the apparent “filling in” of the cup. In contrast to the present study, Irak et al13 found no correlation between age and changes in optic disc parameters; such a correlation may have been absent because they achieved a significantly smaller pressure reduction in their older patients compared with their younger patients. Our patients with advanced cupping seemed to have the same degree of reversibility of HRT optic disc parameters as patients with less advanced cupping. This finding runs counter to findings of several other authors using experimental systems. Shirakashi et al14 looked at spontaneous IOP reduction in five monkey eyes during the first year after induction of glaucoma. They found less reversal of cupping at 9 to 12 months than they had found at 1 to 4 months. Coleman et al15 photographed eight glaucomatous monkey optic discs within 15 minutes of acutely lowering their IOP. The anterior displacement of the optic disc was significantly less in discs with larger and deeper cups. Zeimer et al16 reported that in postmortem human glaucomatous eyes, the optic nerve head compliance decreased as the visual field worsened but correlation was weak. In contrast, Burgoyne et al17 were unable to show a decreased optic disc compliance 13 to 18 weeks after the induction of glaucoma in 26 monkey eyes. The present study differs from these studies in many ways. Subjects were living humans with glaucoma; most patients had had glaucoma for many years; changes were recorded months after IOP reduction; and the subjects were heterogeneous with respect to multiple factors. As well, only two patients had clinical cup:disc ratios of 0.9 or greater, and only one patient had a cup:disc ratio less than 0.6. Therefore, a correlation with cup:disc ratio would have been hard to achieve considering the relatively small sample size. In group B, older patients showed greater reversal of maximum cup depth, mean cup depth, and cup volume than younger patients, independent of degree of IOP reduction. Zeimer et al16 found no significant correlation between age and short-term optic nerve head compliance, but this was in postmortem human glaucomatous eyes. Clinically, reversal of cupping is most marked in children. Interestingly, the parameters most sensitive to age related to cup depth rather than to rim area or volume. The meaning of this observation is unclear and needs confirmation. Sogano et al18 were able to demonstrate significant changes in RNFL height after glaucoma surgery using the Rodenstock Optic Nerve Head Analyzer. In the present study, pressure-dependent changes in RNFL were not statistically significant. Only three patients in the present study were more myopic than ⫺3.0 D. The small sample size would have made a correlation between refraction and optic disc parameter changes difficult to discover, even if one did exist. The thinner sclera in myopes and their increased glaucomatous and peripapillary atrophy would lead one to assume that the myopic optic disc might react differently to IOP reduction. However, we were unable to demonstrate this relationship. Azuara–Blanco et al19 also found no differences between myopic and emmetropic (nonglaucomatous) subjects when HRT parameters are analyzed before and after experimental increases in IOP. Worrisome, however, was the finding in
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Ophthalmology Volume 106, Number 5, May 1999 the present study that among patients having ⬎40% IOP reduction, the only two patients not demonstrating reversal of optic disc parameters were both young high myopes. Whether this finding is of clinical significance remains to be determined. The study suggests that technology may have reached a level of sensitivity where subtle improvement in disc morphology can now be reliably detected. This technology may permit us to evaluate reversal of cupping (rather than simply percent IOP reduction) as a predictor of future stability of glaucomatous optic neuropathy.
References 1. Spaeth GL, Fellman RL, Starita RL, et al. A new management system for glaucoma based on improvement of the appearance of the optic disc or visual field. Trans Am Ophthalmol Soc 1985;83:268 – 84. 2. Katz LJ, Spaeth GL, Cantor LB, et al. Reversible optic disk cupping and visual field improvement in adults with glaucoma. Am J Ophthalmol 1989;107:485–92. 3. Shin DH, Bielik M, Hong YJ, et al. Reversal of glaucomatous optic disc cupping in adult patients. Arch Ophthalmol 1989; 107:1599 – 603. 4. Funk J. Increase of neuroretinal rim area after surgical intraocular pressure reduction. Ophthalmic Surg 1990;21:585– 8. 5. Rohrschneider K, Burk ROW, Kruse FE, Volcker HE. Reproducibility of the optic nerve head topography with a new laser tomographic scanning device. Ophthalmology 1994;101:1044 –9. 6. Janknecht P, Funk J. Optic nerve head analyser and Heidelberg Retina Tomograph: accuracy and reproducibility of topographic measurements in a model eye and in volunteers. Br J Ophthalmol 1994;78:760 – 8. 7. Chauhan BC, LeBlanc RP, McCormick TA, Rogers JB. Test– retest variability of topographic measurements with confocal
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scanning laser tomography in patients with glaucoma and control subjects. Am J Ophthalmol 1994;118:9 –15. Shields MB, Tiedeman JS, Miller KN, et al. Accuracy of topographic measurements with the optic nerve head analyzer. Am J Ophthalmol 1989;107:273–9. Shields MB, Martone JF, Shelton AR, et al. Reproducibility of topographic measurements with the optic nerve head analyzer. Am J Ophthalmol 1987;104:581– 6. Weinreb RN, Lusky M, Bartsch DU, Morsman D. Effect of repetitive imaging on topographic measurements of the optic nerve head. Arch Ophthalmol 1993;111:636 – 8. von Jaeger E. Ophthalmoskopischer Hand-atlas. Wien: K. K. Hof-und Staatsdruckere, 1869. Raitta C, Tomita G, Vesti E, et al. Optic disc topography before and after trabeculectomy in advanced glaucoma. Ophthalmic Surg Lasers 1996;27:349 –54. Irak I, Zangwill L, Garden V, et al. Change in optic disk topography after trabeculectomy. Am J Ophthalmol 1996;122: 690 –5. Shirakashi M, Nanba K, Iwata K. Changes in reversal cupping in experimental glaucoma. Ophthalmology 1992;99:1104 –10. Coleman AL, Quigley HA, Vitale S, Dunkelberger G. Displacement of the optic nerve head by acute changes in intraocular pressure in monkey eyes. Ophthalmology 1991;98:35– 40. Zeimer RC, Ogura Y. The relation between glaucomatous damage and optic nerve head mechanical compliance. Arch Ophthalmol 1989;107:1232– 4. Burgoyne CF, Quigley HA, Thompson HW, et al. Early changes in optic disc compliance and surface position in experimental glaucoma. Ophthalmology 1995;102:1800 –9. Sogano S, Tomita G, Kitazawa Y. Changes in retinal nerve fiber layer thickness after reduction of intraocular pressure in chronic open-angle glaucoma. Ophthalmology 1993;100: 1253– 8. Azuara-Blanco A, Harris A, Cantor LB, et al. Effects of short term increase of intraocular pressure on optic disc cupping. Br J Ophthalmol 1998;82:880 –3.