Intraocular Pressure and Progression of Glaucomatous Visual Field Loss ´ , MD, PHD, BALWANTRAY C. CHAUHAN, PHD, CARLOS MARTI´NEZ-BELLO MARCELO T. NICOLELA, MD, TERRY A. MCCORMICK, BA, AND RAYMOND P. LEBLANC, MD
● PURPOSE:
To evaluate the relationship between intraocular pressure and visual field progression in patients with primary open-angle glaucoma. ● METHODS: We prospectively followed 113 patients with early to moderate glaucomatous field damage. Conventional automated static perimetry, high-pass resolution perimetry, and intraocular pressure measurements were carried out at 6-month intervals. The mean and the highest intraocular pressure in the follow-up were compared in stable and progressing patients with each perimetric technique. ● RESULTS: The mean (ⴞ SD) follow-up was 4.5 ⴞ 0.9 years. The mean (ⴞ SD) intraocular pressure in patients remaining stable with conventional perimetry [18.2 ⴞ 3.3 mm Hg, n ⴝ 81 (71.7%)] was not significantly different (P ⴝ .65) from those in whom it progressed (17.9 ⴞ 3.3 mm Hg, n ⴝ 32 [28.3%]). The mean intraocular pressure in patients remaining stable with high-pass resolution perimetry (17.9 ⴞ 3.5 mm Hg, n ⴝ 63 [55.8%]) was not significantly different (P ⴝ .33) from those in whom it progressed (18.5 ⴞ 3.0 mm Hg, n ⴝ 50 [44.2%]). The mean (ⴞ SD) of the highest (single or three highest) pressure during follow-up for stable and progressing patients with conventional perimetry was not significantly different (22.6 ⴞ 5.0 and 23.0 ⴞ 4.6 mm Hg, respectively, P ⴝ .76). However, for high-pass resolution perimetry, the difference was highly significant (21.6 ⴞ 4.5 and 24.1 ⴞ 4.9 mm Hg, respectively, P < .01). Furthermore, patients who progressed with high-pass resolution perimetry had more damaged baseline fields compared with those who remained stable (P < .01). Accepted for publication Oct 8, 1999. From the Departments of Ophthalmology (Drs Martı´nez-Bello´, Chauhan, Nicolela, McCormick, and LeBlanc) and Physiology and Biophysics (Dr Chauhan), Dalhousie University, Halifax, Nova Scotia, Canada. This study was supported by grant MT-11357 from the Medical Research Council of Canada, Ottawa, Ontario, Canada. Correspondence to Balwantray C. Chauhan, PhD, Department of Ophthalmology, Dalhousie University, 2nd Fl, Centennial Building, 1278 Tower Rd, Halifax, Nova Scotia, Canada B3H 2Y9; fax: (902) 473-2839; e-mail:
[email protected]
302
©
2000 BY
● CONCLUSIONS:
The mean level of intraocular pressure does not differentiate glaucoma patients with progressive visual field loss from ones who remained stable. Baseline visual field status and peak intraocular pressure of patients who progress with high-pass resolution perimetry are significantly different from those who remain stable. (Am J Ophthalmol 2000;129:302–308. © 2000 by Elsevier Science Inc. All rights reserved.)
G
LAUCOMA IS A DISEASE OF THE OPTIC NERVE PRO-
duced by degeneration of the retinal ganglion cells. This glaucomatous optic neuropathy is characterized by atrophy of the optic disk and progressive deterioration of the visual field. Traditionally, these anatomic and functional lesions were considered to be a direct consequence of an elevation of intraocular pressure. The role of intraocular pressure in the pathogenesis of glaucoma has, however, been controversial.1–5 Studies have unequivocally confirmed that individuals with glaucoma have, on average, higher levels of intraocular pressure than those without the disease and that intraocular pressure is a dose-related risk factor.1 Paradoxically, one third to one half of individuals with glaucomatous nerve damage do not show increased intraocular pressure levels,2,3 and as many as 90% of individuals with increased intraocular pressure do not show glaucomatous nerve damage over periods of 5 years4 and 10 years.5 Therefore, increased intraocular pressure appears insufficient to explain the existence of all cases of this disease. Current treatment modalities are oriented toward lowering intraocular pressure levels with the aim of reducing risk of optic disk and visual field progression. However, conflicting evidence exists regarding an intraocular pressure level below which progression of visual field loss does not occur and above which progression always does. Intraocular pressure reductions from 30% to 59%6 –9 and levels below 17 mm Hg10 or 24 mm Hg11 have been reported to be associated with a low incidence of further progression of the visual field, or even its improvement. These and other studies,12,13 have confirmed a significant correlation between the intraocular pressure level and the
ELSEVIER SCIENCE INC. ALL
RIGHTS RESERVED.
0002-9394/00/$20.00 PII S0002-9394(99)00387-6
rate of visual field loss. Conversely, some authors could not find a clear intraocular pressure level that reliably distinguished between glaucoma patients with stable and progressive fields, reporting that many patients experienced further progression of the field despite extensive lowering of the intraocular pressure.14 –22 The likely discrepancy between the intraocular pressure level and presence or absence of progression of visual field damage may be the result of differences in study population and design and may also suggest that other risk factors in addition to intraocular pressure may be responsible for disease progression.19 –22 The purpose of this study was to report the value of intraocular pressure as a predictor of progression of visual field damage in patients with open-angle glaucoma, and to determine whether intraocular pressure can reliably distinguish between stable and progressive patients. There have been a number of retrospective studies examining this relationship. However, our study differs in that it was a prospective study in which patients were tested regularly at six monthly intervals. Furthermore, visual field examinations were performed on each patient using two different perimetric techniques: conventional automated (Humphrey) and high-pass resolution (Ring) perimetry. The latter is a relatively new technique, which has recently been shown to be more sensitive than conventional perimetry at detecting glaucomatous progression.23 We therefore wanted to determine whether there was a difference between the two perimetric techniques regarding the relationship between intraocular pressure and visual field progression.
PATIENTS AND METHODS PATIENTS WITH GLAUCOMA WHO MET THE INCLUSION
and exclusion criteria (Table 1) were recruited on a consecutive basis from the practice of one of us (R.P.L.) and from the Eye Care Centre of the Queen Elizabeth II Health Sciences Centre. This study was approved by the Queen Elizabeth II Health Sciences Centre Ethics Committee. The nature of the procedures was fully explained to each subject. All patients first underwent a complete ophthalmologic examination. When both eyes of one patient were eligible for the study, only one eye, selected randomly, was tested and continued to be the study eye during the follow up. Visual field examinations were performed on each patient with both conventional and high-pass resolution perimetry at each visit. We used program 30-2 of the Humphrey Field Analyser (Humphrey Instruments, Inc, San Leandro, California) for conventional perimetry, and the Ring program of the Opthimus system (High Tech Vision, Go¨teborg, Sweden) for high-pass resolution perimetry, as described previously.24 Unlike conventional perimetry, high-pass resolution perimetry uses stimuli with fixed VOL. 129, NO. 3
INTRAOCULAR PRESSURE
TABLE 1. Inclusion and Exclusion Criteria for the Study Inclusion Criteria ● Diagnosis of chronic open-angle glaucoma with glaucomatous optic disk damage ● Normal open angles by gonioscopy ● Best-corrected visual acuity ⱖ 20/40 ● Visual field damage compatible with glaucoma with a mean deviation index between ⫺2 and ⫺10 dB ● Minimum of five visual fields with conventional and highpass resolution perimetry ● Informed consent to participate in the study Exclusion Criteria ● Systemic disease or systemic medication that affects the visual field ● Concomitant ocular disease ● Refractive error ⬎ 5 diopters equivalent sphere or 3 diopters astigmatism ● Contact lens wear
luminance characteristics but varies stimulus size to measure threshold in 50 locations in the central visual field. The two perimetry examinations were always performed at the same visit, usually after a short rest period, by the same technician. We randomized the type of perimeter to be used first at each visit. All patients had previous experience with conventional perimetry but had not been previously tested with high-pass resolution perimetry. Pupils less than 3 mm in diameter were dilated with tropicamide (0.8%) and phenylephrine (5%) for the perimetric tests. Baseline visual field values for each patient were determined by performing the visual field examination with both techniques (conventional and high-pass resolution perimetry) and repeating these tests 1 week later. Follow-up visits occurred every 6 months thereafter. The reliability of a visual field examination was evaluated partially by using the reliability indexes. However, more emphasis was given to the perimetrist’s comments on each visual field printout. Visual fields that were not judged to be reliable were repeated. Intraocular pressure was measured with a Goldmann applanation tonometer after both perimetric techniques were performed. The mean of three measurements was taken. During follow-up, each patient was treated according to the attending ophthalmologist. Because patients tested with high-pass resolution perimetry may have been subject to a small learning effect between the first two examinations,25 we excluded the first visual field result, using the mean of the 7-day and 6-month examination results as the baseline for each patient. In contrast, we used the 0-day and 7-day visual field with conventional perimetry. We compared subsequent visual fields against these baselines. We used the Glaucoma Change Probability Analysis of the Statpac program26 to analyze progression with conventional perimetry. The mean of two baseline tests is first AND
VISUAL FIELD LOSS
303
calculated followed by pointwise differences between subsequent tests and baselines. At every location, differences in the threshold deviation between follow-up and baseline falling outside the fifth percentile for test–retest variability in stable glaucoma patients are indicated as locations with probable deterioration. To include in the analysis the same number of test points and approximate position in the visual field with each perimetric technique, we removed the edge points from program 30-2 from the analysis, leaving 50 locations analyzed with each technique.23 We devised a similar change probability analysis program for high-pass resolution perimetry using our own test–retest variability data.23 Our predefined criterion for progression was the presence of a minimum of four fully overlapping locations outside the fifth percentile in two of three consecutive examinations. We compared the mean intraocular pressure throughout the follow-up in progressing and stable patients with both perimetric techniques. We also analyzed the highest intraocular pressure during the follow-up. The Student t test and Mann-Whitney test were used for statistical analysis. A P value of less than .05 was considered statistically significant.
FIGURE 1. Frequency distribution of the number of visual field examinations in the follow-up.
was measured with conventional perimetry (Table 2, Figure 4). However, when progression was measured with high-pass resolution perimetry, progressing patients had a significantly greater highest (single or three highest) pressure compared with stable patients (Table 2, Figure 4). They also had a higher standard deviation of pressures during follow-up (Table 2). Other characteristics for the patients are shown in Table 3 and indicate that there were no differences between stable and progressing patients in age, gender distribution, number of perimetric examinations, baseline or final visual acuity, or the number of medications when progression with either technique was considered. However, differences for the level of visual field damage at baseline between stable and progressing patients were significant for high-pass resolution perimetry (P ⬍ .01, Table 3). Although there was a suggestion of a similar finding with conventional perimetry, it reached only borderline significance (P ⫽ .07, Table 3). The fact that we could not detect statistically significant differences in mean intraocular pressure between the groups studied does not necessarily indicate that real differences did not exist. We performed power calculations to ensure that our sample size and intraocular pressure distribution characteristics were sufficient to detect statistically significant differences in mean intraocular pressure, had they existed (Table 4). These calculations show that our study had high and very high statistical power to detect differences in the mean intraocular pressure of 2 and 3 mm Hg, respectively, had they existed.
RESULTS THE STUDY POPULATION CONSISTED OF 113 EYES OF 113
patients, of whom 55 were men and 58 were women. The mean (⫾ SD) age at the beginning of the study was 61.4 ⫾ 13.1 years (range, 17 to 89 years). The patients were followed for a mean (⫾ SD) period of 4.6 ⫾ 0.9 years (range, 2 to 6 years). The mean (⫾ SD) number of visual field examinations (conventional and high-pass resolution perimetry) and intraocular pressure measurements was 10.1 ⫾ 2.4 (range, 5 to 13). The distribution of the number of perimetric examinations is shown in Figure 1. The visual fields of 57 patients (50.4%) remained stable with both perimetric techniques. Twenty-six patients (23%) showed progression with both conventional and high-pass resolution perimetry, 24 (21.2%) showed progression with only high-pass resolution perimetry, and six (5.3%) showed progression with only conventional perimetry (Figure 2). With conventional perimetry, the visual field remained stable in 81 patients (71.7%) and progressed in 32 patients (28.3%), whereas with high-pass resolution perimetry, the visual field remained stable in 63 patients (55.8%) and progressed in 50 patients (44.2%). The mean intraocular pressure during the follow-up for stable and progressing patients, measured with either technique (Table 2, Figure 3), was not statistically significantly different. The mean of either the highest single pressure or the three highest pressures during the follow-up for stable and progressing patients was not significantly different when progression 304
AMERICAN JOURNAL
DISCUSSION OUR STUDY SHOWED THAT PROGRESSION OF VISUAL FIELD
damage in glaucoma, determined by conventional and OF
OPHTHALMOLOGY
MARCH 2000
FIGURE 2. Percentage of stable and progressing patients determined by conventional and high-pass resolution perimetry.
high-pass resolution perimetry, occurs over a wide distribution of intraocular pressure values. We could not find significant differences in the mean intraocular pressure during the follow-up between stable and progressing glaucoma patients using either perimetric technique. Some patients in our study had visual field progression with either technique with mean intraocular pressure levels as low as 13 mm Hg, and conversely, other patients remained stable with mean levels as high as 28 mm Hg during follow-up. This wide variability in intraocular pressure in relation to visual field progression in glaucoma has been documented before.15,20 –22 Our results are not, however, in agreement with some retrospective studies showing that stable and progressing glaucoma patients could be separated based on their pressure characteristics.8 –11 The wide range of intraocular pressure over which we observed stability and progression in the visual field in addition to a lack of a significant group differences between the two groups suggest that factors other than intraocular pressure may contribute to progression in glaucoma.19 –22,27–30 It should be noted that clinically recorded pressure measurements may not adequately reflect the true pressure characteristics over time. However, we are currently limited to single or at best diurnal pressure measurements.
Both static and kinetic perimetric techniques are used clinically to identify and measure glaucomatous visual field damage, as have studies that have examined the relationship between intraocular pressure and field progression. It appears, therefore, that irrespective of the technique employed, conflicting conclusions have been made about this relationship. In our study, we determined glaucomatous visual field damage with conventional and high-pass resolution perimetry. A recent study23 on the same cohort of patients has reported that high-pass resolution perimetry detects glaucomatous progression earlier than conventional perimetry. This finding was judged not to be the result of a nonglaucomatous origin, especially cataract, since the baseline and last-visit visual acuities were not significantly different for stable and progressing patients with either technique. Furthermore, 105 patients (92.9%) maintained an acuity of 20/30 or better.23 The fact that high-pass resolution perimetry is significantly more sensitive than conventional perimetry at identifying progressive visual field damage could explain why the former technique was able to differentiate stable from progressing patients based on the level of visual field
TABLE 2. Intraocular Pressure Characteristics of the Stable and Progressing Groups With Conventional and High-pass Resolution Perimetry* Conventional Perimetry
Mean IOP Standard deviation of IOP Highest IOP Mean of 3 highest IOP
Stable (n ⫽ 81)
Progressing (n ⫽ 32)
18.2 ⫾ 3.3 2.7 ⫾ 1.3 22.6 ⫾ 5.0 21.1 ⫾ 4.3
17.9 ⫾ 3.3 3.1 ⫾ 1.4 23 ⫾ 4.6 21.5 ⫾ 4.0
High-pass Resolution Perimetry
P Value
Stable (n ⫽ 63)
Progressing (n ⫽ 50)
P Value
.65 .67 .76 .70
17.9 ⫾ 3.5 2.4 ⫾ 1.0 21.6 ⫾ 4.5 20.4 ⫾ 4.2
18.5 ⫾ 3.0 3.3 ⫾ 1.6 24.1 ⫾ 4.9 22.3 ⫾ 4.1
.33 ⬍.01 ⬍.01 ⬍.05
IOP ⫽ intraocular pressure. *Data are mean ⫾ standard deviation.
VOL. 129, NO. 3
INTRAOCULAR PRESSURE
AND
VISUAL FIELD LOSS
305
FIGURE 3. Frequency distribution of mean intraocular pressure throughout the follow-up for stable and progressing glaucoma patients determined by conventional perimetry (left) and high-pass resolution perimetry (right).
FIGURE 4. Frequency distribution for highest intraocular pressure recorded in the follow-up for stable and progressing patients determined by conventional perimetry (left) and high-pass resolution perimetry (right).
306
AMERICAN JOURNAL
OF
OPHTHALMOLOGY
MARCH 2000
TABLE 3. Characteristics of the Stable and Progressing Groups With Conventional and High-pass Resolution Perimetry* Conventional Perimetry
Baseline age (years) Gender (male/female) No. of visual field examinations Visual acuity (logMAR) Baseline End of study Baseline MD (dB, ring units) No. of glaucoma medications Baseline End of study
Stable (n ⫽ 81)
Progressing (n ⫽ 32)
61.4 ⫾ 13.2 36/45 9.8 ⫾ 2.7
High-pass Resolution Perimetry
P Value
Stable (n ⫽ 63)
Progressing (n ⫽ 50)
61.3 ⫾ 13.0 19/13 10.6 ⫾ 1.6
.95 .15 .45
60.4 ⫾ 13.9 28/35 9.7 ⫾ 2.7
62.6 ⫾ 12.0 27/23 10.5 ⫾ 1.9
.36 .31 .16
0.15 ⫾ 0.18 0.15 ⫾ 0.22 ⫺4.8 ⫾ 2.5
0.12 ⫾ 0.17 0.14 ⫾ 0.26 ⫺5.9 ⫾ 3.4
.35 .81 .07
0.16 ⫾ 0.18 0.13 ⫾ 0.21 ⫺1.6 ⫾ 1.0
0.14 ⫾ 0.18 0.18 ⫾ 0.25 ⫺2.2 ⫾ 1.0
.52 .23 ⬍.01
1.1 ⫾ 0.8 1.4 ⫾ 1.0
1.3 ⫾ 0.9 1.7 ⫾ 0.8
.36 .14
1.1 ⫾ 0.8 1.3 ⫾ 1.0
1.3 ⫾ 0.8 1.7 ⫾ 0.9
P Value
.39 .06
*Data are mean ⫾ standard deviation.
TABLE 4. Power Calculation (%)* for Detecting Group Differences in Mean Intraocular Pressure Progression With Difference (mm Hg)
Conventional Perimetry
High-pass Resolution Perimetry
1 mm Hg 2 mm Hg 3 mm Hg
29.8 81.9 99.0
36.0 89.2 99.8
*Calculations made with the assumption that type I error (␣) ⫽ 0.05.
damage at start of follow-up and their highest intraocular pressures. This finding regarding highest pressures suggests that patients with higher peak intraocular pressures may be more susceptible to progression. Previous studies10,20,31 have examined the relationship between the highest intraocular pressure and visual field progression with static and kinetic perimetry, but they have found conflicting results. The fact that the same patients were tested with both perimetric techniques, which yielded different results for the highest pressure with respect to stable or progressing fields, reinforces our finding. We also performed a similar analysis using the mean of the three highest intraocular pressures for each patient and obtained similar results. In the present study, we had sufficient statistical power to support our conclusion that mean intraocular pressure during the follow-up does not distinguish stable from progressing patients with either technique. The sample size was large enough and the variability characteristics of intraocular pressure small enough that we would have detected statistically significant group differences, had they existed. Differences of 2 mm Hg would have been detected 81.9 and 89.2 times of 100 using progression criteria with VOL. 129, NO. 3
INTRAOCULAR PRESSURE
conventional and high-pass resolution perimetry, respectively. Differences of 3 mm Hg would have been detected 99.0 and 99.8 times of 100 using progression criteria with conventional and high-pass resolution perimetry, respectively. Most studies on intraocular pressure–visual field correlation are retrospective, and each study has defined inclusion and exclusion criteria differently so that staging of glaucomatous damage and definitions of progression varied significantly and may have contributed to the conflicting findings to date. Our study was prospective and included patients with only mild and moderate visual field damage. The absence, however, of a defined treatment protocol may be a confounding factor that could introduce bias in our results. It is possible that patients identified by the clinician with higher risk for progression may have been treated differently from those with a risk that was perceived to be lower. Our study showed that there is no correlation between intraocular pressure levels and visual field damage progression and, importantly, not that reducing the intraocular pressure is ineffective for slowing or halting further glaucomatous damage. For example, an untreated group under the same scenario may have shown a significantly higher rate of progression. Additionally, it is also possible that a study comparing different levels of pressure reduction may show a beneficial effect of more aggressive therapy. A recent study performed by the Collaborative NormalTension Glaucoma Study Group32 determined that lowering intraocular pressure by 30% reduced the rate of progression even in patients with normal-tension glaucoma compared with untreated control patients. Further prospective studies with clearly defined intraocular pressure treatment protocol in the whole spectrum of patients with glaucoma are now necessary in addition to closer examination of the potential non–pressure-related risk factors. AND
VISUAL FIELD LOSS
307
REFERENCES 17.
1. Sommer A, Tielsch JM, Katz J, et al; Baltimore Eye Survey Research Group. Relationship between intraocular pressure and primary open angle glaucoma among white and black Americans. Arch Ophthalmol 1991;109:1090 –1095. 2. Hollows FC, Graham PA. Intra-ocular pressure, glaucoma and glaucoma suspects in a defined population. Br J Ophthalmol 1966;50:570 –586. 3. Kahn HA, Milton RC. Alternative definitions of open-angle glaucoma: effect on prevalence and associations in the Framingham Eye Study. Arch Ophthalmol 1980;98:2172– 2177. 4. Armaly MF, Krueger DE, Maunder L, et al. Biostatistical analysis of the collaborative glaucoma study. I. Summary report of the risk factors for glaucomatous visual-field defects. Arch Ophthalmol 1980;98:2163–2171. 5. Kitazawa Y, Horie T, Aoki S, Suzuki M, Nishioka K. Untreated ocular hypertension: a long-term prospective study. Arch Ophthalmol 1977;95:1180 –1184. 6. Katz LJ, Spaeth GL, Poryzees EM, Steinnmann WC. Reversible optic disk cupping and visual field improvement in adults with glaucoma. Am J Ophthalmol 1989;107:485– 492. 7. Tsai CS, Shin DH, Wan JY, Zeiter JH. Visual fields global indices in patients with reversal of glaucomatous cupping after intraocular pressure reduction. Ophthalmology 1991; 98:1412–1419. 8. Kolker AE. Visual prognosis of advanced glaucoma: a comparison of vision in 101 eyes with advanced glaucoma. Trans Am Ophthalmol Soc 1977;75:539 –555. 9. Quigley HA, Maumenee AE. Long-term follow-up of treated open-angle glaucoma. Am J Ophthalmol 1979;87:519 –525. 10. Mao LK, Stewart WC, Shields MB. Correlation between intraocular pressure control and progressive glaucomatous damage in primary open-angle glaucoma. Am J Ophthalmol 1991;111:51–55. 11. Kass MA, Kolker AE, Becker B. Prognostic factors in glaucomatous visual field loss. Arch Ophthalmol 1976;94: 1274 –1276. 12. Spaeth GL. The effect of change in intraocular pressure on the natural history of glaucoma: lowering intraocular pressure in glaucoma can result in improvement of visual fields. Trans Ophthalmol Soc UK 1985;104:256 –264. 13. Vogel R, Crick RP, Newson RB, Shipley M, Blackmore H, Bulpitt CJ. Association between intraocular pressure and loss of visual field in chronic simple glaucoma. Br J Ophthalmol 1990;74:3– 6. 14. Schultz JS, Werner EB, Krupin T, Bishop KI, Koelle J. Intraocular pressure and visual field defects after argon laser trabeculoplasty in chronic-open angle glaucoma. Ophthalmology 1987;94:553–557. 15. Kidd MN, O’Connor M. Progression of field loss after trabeculectomy: a five-year follow-up. Br J Ophthalmol 1985;69:827– 831. 16. Popovic V, Sjostrand J. Long-term outcome following tra-
18. 19. 20. 21. 22. 23.
24.
25.
26.
27. 28. 29. 30. 31. 32.
beculectomy: II. Visual field survival. Acta Opthalmol (Copenh) 1991;69:305–309. Schulzer M, Mikelberg FS, Drance SM. Some observations on the relation between intraocular pressure and the progression of glaucomatous visual loss. Br J Ophthalmol 1987;71: 486 – 488. O’Brien C, Schwartz B, Takamoto T, Wu DC. Intraocular pressure and the rate of visual field loss in chronic open-angle glaucoma. Am J Ophthalmol 1991;111:491–500. Schulzer M, Drance SM, Douglas GR. A comparison of treated and untreated glaucoma suspects. Ophthalmology 1991;98:301–307. Chauhan BC, Drance SM. The relationship between intraocular pressure and visual field progression in glaucoma. Graefes Arch Clin Exp Ophthalmol 1992;230:521–526. Odberg T. Visual field prognosis in early glaucoma: a longterm clinical follow-up. Acta Ophthalmol (Copenh) 1993; 71:721–726. The AGIS Investigators. The advanced glaucoma intervention study (AGIS): 4. Comparison of treatment outcomes within race. Ophthalmology 1998;105:1146 –1164. Chauhan BC, House PH, McCormick TA, LeBlanc RP. Comparison of conventional and high-pass resolution perimetry in a prospective study of patients with glaucoma and normal controls. Arch Ophthalmol 1999;117:24 –33. Frise´n L. A computer-graphics visual field screener using high-pass spatial frequency resolution targets and multiple feedback devices. Doc Ophthalmol Proc Ser 1987;49:441– 446. Drance SM, Douglas GR, Schulzer M, Wijsman CS. The learning effect of the Frise´n high–pass resolution perimeter. In: Heijl A, editor. Perimetry update 1988/89. Amsterdam: Kugler & Ghedini, 1989:199 –201. Heijl A, Lindgren G, Lindgren A,et al. Extended empirical statistical package for evaluation of single and multiple fields: Statpac 2. In: Mills RP, Heijl A, editors. Perimetry update 1990/1991. New York: Kugler & Ghedini, 1991:303–315. Anderson DR. Glaucoma: the damage caused by pressure. XLVI Edward Jackson Memorial Lecture. Am J Ophthalmol 1989;108:485– 495. Schumer RA, Podos SM. The nerve of glaucoma! Arch Ophthalmol 1994;112:37– 44. Brubaker RF. Delayed functional loss in glaucoma. LII Edward Jackson Memorial Lecture. Am J Ophthalmol 1996; 121:473– 483. Drance SM. Glaucoma: a look beyond intraocular pressure. Am J Ophthalmol 1997;123:817– 819. Werner EB, Drance SM, Schulzer M. Trabeculectomy and the progression of glaucomatous visual field loss. Arch Ophthalmol 1977;5:1374 –1377. The Collaborative Normal-Tension Glaucoma Study Group. Comparison of glaucomatous progression between untreated patients with normal-tension glaucoma and patients with therapeutically reduced intraocular pressures. Am J Ophthalmol 1998;126:487– 497.
The full-text of AJO is now available online at www.ajo.com. Authors Interactive威, currently available in limited form, is undergoing an upgrade.
308
AMERICAN JOURNAL
OF
OPHTHALMOLOGY
MARCH 2000
