Abstract
purpose. To identify progressive rim loss and describe patterns of regional change in various clinical presentations of glaucoma by scanning laser tomography (SLT).
methods. A previously described analytical approach was used to identify progressive rim area loss in SLT disc images of eyes of people with ocular hypertension (OHT, n = 97), early POAG (OHT converters; n = 30), asymmetric normal-pressure glaucoma (NPG, established and suspected in contralateral eyes; n = 26), and normal control subjects (n = 32). Analysis was performed longitudinally in individual image series, and cross-sectionally within groups at different time points.
results. Reproducibly reduced rim area was detected in 2 (6.2%) of 32 normal control subjects, 11 (11%) of 97 OHT subjects, 27 (90%) of 30 OHT converters, 16 (58%) of 26 of suspected NPG eyes, and 15 (54%) of 26 of established NPG eyes (mean MD = −6.5 dB). Of 5 (19%) of 26 of suspected NPG eyes that converted on visual field testing, rim loss was detected in 3 of 5. In all groups, rim loss was common in the disc poles, especially inferiorly. Patterns of rim loss were similar within high-pressure and normal-pressure groups, whether or not eyes had field defects in each. In high-pressure groups, rim loss was more common nasally than temporally. Normal-pressure groups, unlike high-pressure groups, frequently had rim loss temporally. Suspected NPG eyes had more rim loss temporally and their rim area tended to be less compared with OHT and OHT converters, despite the three groups having equivalent baseline fields.
conclusions. There were similarities and differences in the pattern of rim loss in SLT disc images of high- and normal-pressure presentations of glaucoma. Progressive rim loss was detected in eyes without visual field defects, eyes that progressed to develop field defects, and eyes with established and more severe glaucoma.
Sequential neuroretinal rim loss in progressive glaucoma has been described quite extensively by optic disc photography
1 2 3 4 but not as much by the newer technique of scanning laser tomography. Unlike disc photography,
5 6 7 scanning laser tomography data are reproducible
8 9 and amenable to objective and quantitative analysis in a way that could be useful for detecting glaucoma progression.
10 11 12 13
Previous longitudinal photographic studies of neuroretinal rim loss have mostly been in eyes with ocular hypertension (OHT) progressing to develop visual field abnormality.
1 2 4 14 At this stage of disease, the observed pattern of disc cupping is predominantly that of generalized expansion or vertical elongation. In the latter, rim loss inferiorly and superiorly exceeds change nasally and temporally so that the optic disc seems preferentially affected in its poles. Cross-sectional studies agree that the cup commonly becomes vertically oval in “early” glaucoma.
15 16 17 The nature of rim loss in more advanced glaucoma has been understood by cross-sectional studies. Jonas et al.
17 have suggested that rim loss at a given stage of primary open angle glaucoma (POAG) may involve any region of the optic disc, although the location of most pronounced loss varies with the severity of disease.
Concerning the pattern of glaucomatous optic disc change seen in scanning laser tomography, two longitudinal studies are notable. Kamal et al.
18 examined OHT and OHT converter
19 disc images, and suggested a preponderance of change in the superior and inferior regions of the rim and cup. Burgoyne et al.
10 analyzed disc images of monkeys with experimental glaucoma and identified vertical cup-disc ratio and temporal and superior peripapillary retinal height as useful regional parameters for modeling change.
We have described an analytical approach for identifying sequential rim loss in scanning laser tomography that appears reliable enough to distinguish eyes with glaucoma progression from unchanging eyes.
12 13 By analyzing rim loss sector by sector, regional patterns of change within the optic disc can be identified. Based on this, we wondered whether, and in what form, glaucoma progression in various clinical presentations of the disease could be identified by scanning laser tomography. We assessed longitudinal optic disc image series of persons with suspected glaucoma with no field defects (OHT and normal-pressure glaucoma [NPG suspects]), eyes in which perimetrically confirmed high-pressure glaucoma (POAG) developed, and eyes with moderately advanced NPG. Groups were also compared cross-sectionally at the start and end of the follow-up. We then described patterns of regional rim change, compared this between groups, and examined whether identified patterns corresponded in any way to foregoing descriptions derived by standard disc photography.
The analytical approach was tested bilaterally in OHT subjects, bilaterally in asymmetric NPG subjects, the eye that “converted” in OHT converters to POAG, and unilaterally in normal control subjects. The same OHT converters and normal control subjects had been used in a previous publication to test (but not derive) the analytical approach.
13 Subjects attended either the ocular hypertension and early glaucoma, or normal-pressure glaucoma research clinics at Moorfields Eye Hospital. All had received imaging on at least four separate occasions over a minimum of 3 years. Except for NPG eyes, disc appearance was not part of the study’s recruitment criteria. This study adhered to the tenets of the Declaration of Helsinki, having appropriate institutional review board approval and the subjects’ informed consent.
Subjects with OHT had (1) intraocular pressure (IOP) consistently more than 21 mm Hg in one or both eyes without IOP-lowering treatment, (2) open angles on gonioscopy, (3) no defects on at least three consecutive visual field tests (Humphrey Retinal Field Analyzer 24-2 program; Carl Zeiss Meditec, Dublin, CA) with Advanced Glaucoma Intervention Study (AGIS)
20 scores of zero, (4) refractive errors less than ±6 D, (5) no concurrent eye disease or previous intraocular surgery, and (6) age more than 40 years. Eyes of
OHT converters had developed reproducible field defects, as defined by AGIS criteria (score >0), in the same location on three consecutive tests. OHT converters were taken to have early and progressive POAG.
To have asymmetric NPG, both eyes of subjects had (1) untreated mean IOP on phasing of less than 22 mm Hg, with no single reading exceeding 23 mm Hg; (2) gonioscopically open drainage angles; (3) no concurrent ocular disease, previous intraocular surgery or any secondary cause for raised IOP; (4) only one eye had reproducible visual field abnormality at baseline and glaucomatous cupping compatible with the field defect (established NPG); while (5) the contralateral eye had no field defects (suspected NPG). Over the follow-up, in some eyes with suspected NPG reproducible defects developed, and they became NPG converters. Visual field abnormality in asymmetric NPG subjects was defined as for OHT converters. Abnormality was present in an eye only if its visual field received an AGIS score of 1 or more which could be verified as repeatable in the same location on three consecutive field tests. Only then was a field defect accepted as confirmed.
Eyes of normal control subjects were taken to be unchanging. Normal subjects were volunteers comprising spouses or friends of hospital patients, hospital staff, or members of external nonmedical social organizations. They had (1) IOP repeatedly less than 22 mm Hg, (2) serially normal and reliable Humphrey 24-2 visual fields with AGIS field scores of zero, (3) no concurrent ocular disease or previous intraocular surgery, (4) no family history of glaucoma, (5) refractive errors less than ± 6 D, and were (6) aged more than 40 years.
This approach is described in detail elsewhere.
12 13 Briefly, 30° rim area sectors were evaluated for change. The parameter of rim area was evaluated within longitudinal image series using a new experimental reference plane
21 to define the inner edge of the rim. By this reference plane, rim area measurement variability is less and not appreciably affected by glaucoma or testing involving different operators and visits compared with conventional reference planes used in the Heidelberg Retina Tomograph (HRT; Heidelberg Engineering, Heidelberg, Germany).
21 22 23 This makes variability easier to estimate and account for.
The outer extent of the rim coincided with the contour line marking the inner margin of the scleral ring of Elschnig. The same observer drew the contour line in each subject’s baseline mean topography image (JT). Mean images were derived from triplets of single topography images using the HRT software (ver. 2.01; Heidelberg Engineering). Contour lines were exported from a baseline mean topography image to other mean and single topography images in each series. Only images with mean pixel SD < 50 μm were used, and images having a grainy honeycombed appearance were excluded.
For any image series, limits of variability per sector (VARLIM) were calculated according to
\[\mathrm{VARLIM}a\ {=}\ Y\ {\cdot}\ {\surd}{\sum}({\delta}i\ {-}\ X)^{2}/(n\ {-}\ 1)\]
where,
a is the sector number (corresponding to the order of a sector’s location on the disc circumference between 0° and 360°, δ is the sector rim area difference between pairs of intravisit single topography images,
i is the ith value of δ,
X is the mean of observations of δ,
n is the number of observations of δ;
Y is the value of the
t statistic for degrees of freedom for δ, corresponding to a chosen two-tailed probability. A probability level of 0.10 corresponding to a 90% limit of variability was used based on previous findings.
12
Rim area data from each mean topography image were expressed as a
rim area profile. A rim area profile is a plot of a disc’s 30° rim area sectors (in square millimeters) by their angular locations around the disc circumference (0–360°, with 0° temporal, 90° superior, 180° nasal, and 270° inferior), as shown in
Figures 2 3 and 4 . An eye’s longitudinal image data were plotted as sequential rim area profiles in a common graph, each symbol- and color-coded to represent rim area measurement at a specific point in time.
Limits of variability define the extent of measurement variability for an image series with respect to the baseline measurement of rim area. The lower limits of variability for rim area sectors were plotted relative to the baseline rim area profile, with the region beneath the lower limits termed the zone of change. Any rim area sector that diminished, exceeded its lower limit of variability, and entered the zone of change was considered to have changed more than variability alone. This was tentatively taken to represent glaucomatous change. Only sector change repeatedly exceeding variability in two of three sequential tests was confirmed as progression. Data from any number of visits over time, as expressed in sequential rim area profiles, can be simultaneously assessed and weighed against their own variability estimates. An eye was considered to have confirmed progression if at least one of its rim sectors showed repeatable change meeting this criterion.
Analyzing Longitudinal Image Series by the Analytical Approach.
Cross-sectional Analysis of Diagnostic Groups at Baseline and Final Follow-Up.
Two of 32 normal control eyes had repeatable change in at least one rim area sector, giving an estimated false-positive rate of 6.2%.
Of 97 OHT subjects, repeatable rim loss was identified in one eye each of 11 (11%) subjects. By definition, all had no field defects at baseline and final follow-up.
Figure 1A shows that changed sectors were most frequently identified in the inferior pole (240–300°), followed by superiorly (60–90°), and nasally (150–210°). Three (27%) of 11 had rim loss nasally–horizontally (150–210°), but temporal–horizontal change was rare.
Figure 2 is an example of superior–temporal rim loss.
Figure 3 shows diffuse rim loss.
Repeatable rim loss was identified in 27 of 30 OHT converters.
Figure 1B shows that rim loss was most frequently in the inferior pole (270–300°), followed by superotemporal loss between 30° and 90°. Forty-two percent (13/31) had rim loss nasally–horizontally (150–210°), but rim loss temporally–horizontally (330–360°, 0–30°) was rare. Twenty-three (77%) of 30 converters had nasal visual field defects, whereas 2 (6.7%) of 30 had paracentral field defects.
In suspected NPG, rim loss was identified in 15 (58%) of 26 eyes. In 5 (19%) of 26 eyes reproducible field abnormality developed over follow-up, and these eyes were considered NPG converters. Visual fields of the other 21 of 26 eyes remained normal throughout.
Figure 4 shows widespread temporal rim loss and concurrent inferior and inferonasal change in a suspected NPG eye that retained normal visual fields.
Figure 1C shows that rim loss in suspected NPG was most frequently in the inferior pole (270–300°) and temporally–horizontally (0–30°). Nasal rim loss was relatively uncommon.
Of NPG converters, repeatable rim change was confirmed in three of five eyes. One of five eyes had tentative change which, for lack of follow-up data, could not be confirmed. Three (60%) of five NPG converters exhibited paracentral defects at conversion.
In established NPG, 14 (54%) of 26 of eyes had repeatable rim loss.
Figure 1D shows that rim loss was most frequent inferotemporally (300–330°) and temporally–horizontally (330–360°), followed by superotemporally (30–60°) and in the inferior pole (240–300°). As in suspected NPG, but unlike OHT and OHT converter eyes, nasal rim loss was relatively infrequent.
The analytical approach for identifying progressive rim loss was applied to images of eyes with different clinical presentations of glaucoma, as defined by IOP and visual field status. To provide a firm basis for interpreting change in these eyes, we first quantified the performance of the test to establish an acceptable and robust reference standard against which subsequent findings could be interpreted. We did this by assessing unchanging eyes and eyes with unambiguous change, for which we chose normal control subjects and OHT converters, respectively. This then provided a framework for interpreting the approach’s results in eyes whose fields were apparently normal (but suspected of changing, vis-à-vis OHT and suspected NPG) or already had confirmed abnormality (established NPG), in which change might be difficult to detect unambiguously. Difficulty reliably interpreting glaucomatous progression in fields with preexisting defects is well acknowledged.
24 25 26
Based on longitudinally analyzing the images of normal control subjects and OHT converters by 90% limits of variability and the two-of-three criterion, and assuming no change in the former and progression in the latter, repeatable rim loss was identified with a sensitivity of 90% and a false-positive rate of 6.2%. By the same analytical approach, rim loss was identified in three of five NPG converters in whom field defects developed. In eyes with established NPG and moderately severe disease, rim loss was identified in 54%. Repeatable rim loss was also detected even in the absence of field abnormalities: in 52% (11/21) of suspect NPG eyes that retained normal fields and unilaterally in 11% (11/97) of OHT eyes. Patterns of change were then documented in the various diagnostic categories.
The longitudinal and cross-sectional analyses agreed that similar patterns of rim loss were seen in OHT and OHT converters having “early” glaucoma. Rim loss was frequently detected in the disc poles, especially inferiorly, and is consistent with a pattern of the cup elongating vertically. These findings concur with longitudinal
1 4 and cross-sectional
15 16 17 photographic studies of the disc in OHT and conversion. Preferential rim loss at or near the disc poles has been associated clinically with the common location of disc hemorrhages,
27 28 localized nerve fiber layer atrophy,
29 and early field defects
30 and histologically with the configuration of lamina cribrosa pores.
31 32 That concentric cupping may be relatively common in OHT converters
1 4 was reflected in our findings, too. The not uncommon pattern of nasal rim loss seen in OHT and OHT converters suggests that cupping does not occur solely vertically. Still, the overall pattern of change would have been strongly influenced by the preponderance of rim loss in the disc poles. Also, as the normal cup tends to be horizontally oval, more vertical than horizontal rim tissue would have to be lost for cupping to appear concentric in “early” disease.
33 34 Thus, initially, cupping that appears concentric may actually be due to vertical rim loss exceeding horizontal loss. Such a pattern of loss may not be easy to detect by subjective assessment, however,
34 as illustrated in
Figure 2 .
Some patterns were common to all groups. As with high-pressure presentations (OHT and OHT converters with IOP > 21 mm Hg), normal-pressure groups (suspected and established) quite frequently had moderate to large and significant rim loss in the disc poles, especially inferiorly. Patterns of change were similar within high-pressure groups, whether or not field defects were present, and the same held true for normal-pressure presentations. Rim loss was identified in similar proportions of eyes with suspected NPG and established NPG (50–60% in each).
But there were some differences. Unlike high-pressure groups, rim loss in normal-pressure presentations was commonly seen temporally but not nasally, both in longitudinal and cross-sectional analyses. It could be that the relatively large and frequent temporal rim change in established NPG was due to more severe disease (mean MD = −6.5 dB, mean CPSD = 9.9 dB), as Jonas et al.
17 suggest to be the case. NPG suspects, however, had baseline fields that were normal and equivalent to those of OHT and OHT converter eyes, and yet they still had relatively frequent temporal rim loss. The temporal rim loss in NPG seemed to correlate with what was observed of their visual fields: paracentral field defects were found at conversion in 3 of 5 NPG converters, but only 2 (6.7%) of 30 OHT converters. OHT converters had predominantly nasal field defects (77%). Sixty-five percent of eyes with established NPG had paracentral field defects. Several investigators have found that field defects tend to be closer to fixation in NPG than in POAG,
35 36 37 38 and in suspected NPG compared with OHT.
39 We also found that sector rim area deviations from normal were larger and more often significant in suspected NPG than in OHT or OHT converters, suggesting that suspected NPG discs were more cupped at baseline and final follow-up, despite the groups having equivalent fields initially. Other investigators have reported more cupping in NPG than POAG for the same amount of field damage.
35 36 40 41
Using an objective analytical approach for detecting progressive rim loss, common patterns of change were observed within high- and normal-pressure presentations of glaucoma. There was agreement between the patterns of change identified in longitudinal analysis by this approach and those yielded by cross-sectional analyses of the same groups over time. Apparent similarities but also differences were seen between groups, and these correlated with previously published photographic findings. Our longitudinal analysis identified progression in eyes with suspected glaucoma without visual field defects, eyes that progressed to development of definite field defects, and eyes with established and more severe glaucoma.
Supported by the Frances and Renee Hock Trust, Moorfields Eye Hospital, and the International Glaucoma Association, London, United Kingdom (JCHT).
Submitted for publication November 14, 2003; revised January 21, 2004; accepted February 9, 2004.
Disclosure:
J.C.H. Tan, None;
D. Poinoosawmy, None;
R.A. Hitchings, None
The publication costs of this article were defrayed in part by page charge payment. This article must therefore be marked “
advertisement” in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Corresponding author: Roger A. Hitchings, Research and Development, Moorfields Eye Hospital, City Road, London EC1V 2PD, UK;
[email protected].
Mean (SD) | Normal | OHT | Converters | NPG Suspect. | NPG Estab. |
n | 32 | 11 | 30 | 26 | 26 |
Age (y) | 66.2 (10.8) | 65.5 (5.54) | 63.6 (4.79) | 64.4 (8.0) | 64.4 (8.0) |
Follow up (y) | 5.7 (0.85) | 6.0 (0.56) | 6.2 (0.52) | 5.8 (0.73) | 5.8 (0.73) |
MD start (dB) | +0.35 (1.18) | −0.73 (2.12) | −0.75 (1.09) | −0.12 (1.23) | −6.16 (5.09) |
MD end (dB) | +0.30 (1.64) | +0.25 (2.03) | −2.82 (1.88) | −0.37 (1.63) | −6.54 (9.02) |
CPSD start (dB) | 0.88 (0.72) | 1.39 (1.43) | 1.64 (0.86) | 1.33 (1.21) | 7.27 (4.56) |
CPSD end (dB) | 0.96 (0.51) | 1.90 (1.92) | 4.02 (1.27) | 1.82 (1.07) | 9.93 (3.51) |
Rim area start (mm2) | 1.48 (0.30) | 1.26 (0.30) | 1.30 (0.35) | 1.21 (0.35) | 1.10 (0.37) |
Rim area end (mm2) | 1.49 (0.30) | 1.22 (0.34) | 1.24 (0.26) | 1.17 (0.33) | 1.10 (0.38) |
Disc area (mm2) | 1.92 (0.39) | 1.90 (0.35) | 1.83 (0.43) | 1.99 (0.34) | 2.01 (0.42) |
Sommer A, Pollack I, Maumenee AE. Optic disc parameters and onset of glaucomatous field loss. 1: methods and progressive changes in disc morphology. Arch Ophthalmol. 1980;9:1444–1448.
Pederson JE, Anderson DR. The mode of progressive disc cupping in ocular hypertension and glaucoma. Arch Ophthalmol
. 1980;98:490–495.
[CrossRef] [PubMed]Motolko M, Drance SM. Features of the optic disc in preglaucomatous eyes. Arch Ophthalmol
. 1981;99:1992–1994.
[CrossRef] [PubMed]Tuulonen A, Airaksinen PJ. Initial glaucomatous optic disk and retinal nerve fiber layer abnormalities and their progression. Am J Ophthalmol
. 1991;111:485–490.
[CrossRef] [PubMed]Kahn HA, Leibowitz H, Ganley JP, et al. Randomized controlled clinical trial. National Eye Institute workshop for ophthalmologists. Standardizing diagnostic procedures. Am J Ophthalmol
. 1975;79:768–775.
[CrossRef] [PubMed]Lichter PR. Variability of expert observers in evaluating the optic disc. Trans Am Ophthalmol Soc. 1977;74:532–572.
Varma R, Steinmann WC, Scott IU. Expert agreement in evaluating the optic disc for glaucoma. Ophthalmology
. 1992;99:215–221.
[CrossRef] [PubMed]Dreher AW, Tso PC, Weinreb RN. Reproducibility of topographic measurements of the normal and glaucomatous optic nerve head with the laser tomographic scanner. Am J Ophthalmol
. 1991;111:221–229.
[CrossRef] [PubMed]Rohrschneider K, Burk RO, Kruse FE, et al. Reproducibility of the optic nerve head topography with a new laser tomographic scanning device. Ophthalmology
. 1994;101:1044–1049.
[CrossRef] [PubMed]Burgoyne CF, Mercante DE, Thompson HW. Change detection in regional and volumetric disc parameters using longitudinal confocal scanning laser tomography. Ophthalmology
. 2002;109:455–466.
[CrossRef] [PubMed]Chauhan BC, McCormick TA, Nicolela MT, et al. Optic disc and visual field changes in a prospective longitudinal study of patients with glaucoma: comparison of scanning laser tomography with conventional perimetry and optic disc photography. Arch Ophthalmol
. 2001;119:1492–1499.
[CrossRef] [PubMed]Tan JCH, Hitchings RA. Optimizing and validating an approach for identifying glaucomatous change in optic nerve topography. Invest Ophthalmol Vis Sci. .In press
Tan JCH, Hitchings RA. An approach for detecting glaucomatous optic nerve progression by scanning laser tomography. Invest Ophthalmol Vis Sci
. 2003;44:2621–2626.
[CrossRef] [PubMed]Odberg T, Riise D. Early diagnosis of glaucoma: the value of successive stereophotography of the optic disc. Acta Ophthalmol (Copenh)
. 1985;63:257–263.
[PubMed]Read RM, Spaeth GL. The practical clinical appraisal of the optic disc in glaucoma: the natural history of cup progression and some specific disc-field correlations. Trans Am Acad Ophthalmol Otolaryngol
. 1974;78:OP255–OP274.
[PubMed]Kirsch RE, Anderson DR. Clinical recognition of glaucomatous cupping. Am J Ophthalmol
. 1973;75:442–454.
[CrossRef] [PubMed]Jonas JB, Fernandez MC, Sturmer J. Pattern of glaucomatous neuroretinal rim loss. Ophthalmology
. 1993;100:63–68.
[CrossRef] [PubMed]Kamal D, Garway-Heath DF, Hitchings RA, et al. Use of sequential Heidelberg retina tomograph images to identify changes at the optic disc in ocular hypertensive patients at risk of developing glaucoma. Br J Ophthalmol
. 2000;84:993–998.
[CrossRef] [PubMed]Kamal DS, Viswanathan AC, Garway-Heath DF, Hitchings RA, Poinoosawmy D, Bunce C. Detection of optic disc change with the Heidelberg retina tomograph before confirmed visual field change in ocular hypertensives converting to early glaucoma. Br J Ophthalmol
. 1999;83:290–294.
[CrossRef] [PubMed] The AGIS investigators. Advanced Glaucoma Intervention Study 2. Visual field test scoring and reliability. Ophthalmology
. 1994;101:1445–1455.
[CrossRef] [PubMed]Tan JCH, Hitchings RA. Reference plane definition and reproducibility in optic nerve head images. Invest Ophthalmol Vis Sci
. 2003;44:1132–1137.
[CrossRef] [PubMed]Tan JCH, Garway-Heath DF, Hitchings RA. Reasons for rim area variability in scanning laser tomography. Invest Ophthalmol Vis Sci
. 2003;44:1126–1131.
[CrossRef] [PubMed]Tan JCH, Garway-Heath DF, Fitzke FW, Hitchings RA. Variability across regions of the optic nerve head in scanning laser tomography. Br J Ophthalmol
. 2003;87:557–559.
[CrossRef] [PubMed]Schulzer M. Errors in the diagnosis of visual field progression in normal-tension glaucoma. Ophthalmology
. 1994;101:1589–1595.
[CrossRef] [PubMed]Werner EB. In discussion of: Schulzer M, and the Normal Tension Glaucoma Study Group. Errors in the diagnosis of visual field progression in normal tension glaucoma. Ophthalmology. 1994;101:1595.
Tan JCH, Franks WA, Hitchings RA. Interpreting glaucoma progression by white-on-white perimetry. Graefes Arch Clin Exp Ophthalmol
. 2002;240:585–592.
[CrossRef] [PubMed]Airaksinen PJ, Mustonen E, Alanko HI. Optic disc hemorrhages: analysis of stereophotographs and clinical data of 112 patients. Arch Ophthalmol
. 1981;99:1795–1801.
[CrossRef] [PubMed]Jonas JB, Xu L. Optic disk hemorrhages in glaucoma. Am J Ophthalmol
. 1994;118:1–8.
[CrossRef] [PubMed]Airaksinen PJ, Mustonen E, Alanko HI. Optic disc haemorrhages precede retinal nerve fibre layer defects in ocular hypertension. Acta Ophthalmol (Copenh)
. 1981;59:627–641.
[CrossRef] [PubMed]Heijl A, Lundqvist L. The location of earliest glaucomatous visual field defects documented by automatic perimetry. Greve EL Heijl A eds. Fifth International Visual Field Symposium. 1983;153–158. Dr. W. Junk The Hague, The Netherlands.
Quigley HA, Hohman RM, Addicks EM, et al. Morphologic changes in the lamina cribrosa correlated with neural loss in open-angle glaucoma. Am J Ophthalmol
. 1983;95:673–691.
[CrossRef] [PubMed]Pederson JE, Gaasterland DE. Laser-induced primate glaucoma. I. Progression of cupping. Arch Ophthalmol
. 1984;102:1689–1692.
[CrossRef] [PubMed]Airaksinen PJ, Tuulonen A, Werner EB. Clinical evaluation of the optic disc and retinal nerve fiber layer. Ritch R Shields MB Krupin T eds. The Glaucomas. 1996; Mosby St. Louis.
Spaeth GL. Development of glaucomatous changes of the optic nerve. Varma R Spaeth GL eds. The Optic Nerve in Glaucoma. 1993; J.B. Lippincott Philadelphia.
Levene RZ. Low tension glaucoma: a critical review and new material. Surv Ophthalmol
. 1980;24:621–664.
[CrossRef] [PubMed]Gramer E, Althaus G, Leydhecker W. Site and depth of glaucomatous visual field defects in relation to the size of the neuroretinal edge zone of the optic disk in glaucoma without hypertension, simple glaucoma, pigmentary glaucoma: a clinical study with the Octopus perimeter 201 and the optic nerve head analyzer (in Germany). Klin Monatsbl Augenheilkd
. 1986;189:190–198.
[CrossRef] [PubMed]Hitchings RA, Anderton SA. A comparative study of visual field defects seen in patients with low-tension glaucoma and chronic simple glaucoma. Br J Ophthalmol
. 1983;67:818–821.
[CrossRef] [PubMed]Caprioli J, Spaeth GL. Comparison of visual field defects in the low-tension glaucomas with those in the high-tension glaucomas. Am J Ophthalmol
. 1984;97:730–737.
[CrossRef] [PubMed]Poinoosawmy D, McNaught AI, Fitzke FW, et al. Location of early field deterioration in glaucoma suspects. Mills RP Wall M eds. Perimetry Update. 1995;289–297. Kugler Amsterdam/New York.
Caprioli J, Spaeth GL. Comparison of the optic nerve head in high- and low-tension glaucoma. Arch Ophthalmol
. 1985;103:1145–1149.
[CrossRef] [PubMed]Fazio P, Krupin T, Feitl ME, et al. Optic disc topography in patients with low-tension and primary open angle glaucoma. Arch Ophthalmol
. 1990;108:705–708.
[CrossRef] [PubMed]