Abstract

An image analysis method to measure retinal nerve fiber layer (RNFL) striations from digitized fundus photographs was developed to improve detection and monitoring of progressive diffuse RNFL loss. Striations were measured by comparing the high spatial frequency variability across with the variability along the RNFL. This locally normalized measure of striations compensates for the wide density variations both within individuals and between individuals and RNFL photographs. Five repeated measurements were taken at each of three locations from each retinal image. Measurements from five patients with recorded visual field loss due to optic nerve diseases were compared with five normal subjects and five suspect eyes. Measurements clearly distinguished the three groups when taken at the temporal arcades. Measurements above and below the arcades were also consistent, but did not distinguish normals from suspects. The measure was correlated with graded estimates of RNFL integrity of two trained observers (ρ = −0.57, p <0.001 and ρ = −0.61, p < 0.001).

© 1989 Optical Society of America

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References

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  1. W. F. Hoyt, L. Frisén, N. M. Newman, “Funduscopy of Nerve Fiber Layer Defects in Glaucoma,” Invest. Ophthalmol. 12, 814 (1973).
    [PubMed]
  2. A. Vannas, C. Raitta, S. Lemberg, “Photography of the Nerve Fiber Layer in Retinal Disturbances,” Acta Ophthalmol. 55, 79 (1977).
  3. M. Lundström, L. Frisén, “Atrophy of Optic Nerve Fibres in Compression of the Chiasm; Degree and Distribution of Ophthalmoscopic Changes,” Acta Ophthalmol. 54, 623 (1976).
  4. A. Sommer et al., “Evaluation of Nerve Fiber Layer Assessment,” Arch. Ophthalmol. 102, 1766 (1984).
    [CrossRef] [PubMed]
  5. A. Sommer, S. A. D’Anna, H. A. Kues, T. George, “High-Resolution Photography of the Retinal Nerve Fiber Layer,” Am. J. Ophthalmol. 96, 535 (1983).
    [PubMed]
  6. A. Sommer et al., “Cross-Polarization Photography of the Nerve Fiber Layer,” Arch. Ophthalmol. 102, 864 (1984).
    [CrossRef] [PubMed]
  7. P. J. Airaksinen, H. Nieminen, E. Mustonen, “Retinal Nerve Fiber Layer Photography with a Wide Angle Fundus Camera,” Acta Ophthalmol. 60, 362 (1982).
  8. E. Peli et al., “Nerve Fiber Layer Photography: a Comparative Study,” Acta Ophthalmol. 65, 71 (1987).
  9. E. Peli, T. R. Hedges, B. Schwartz, “Computerized Enhancement of Retinal Nerve Fiber Layer,” Acta Ophthalmol. 64, 113 (1986).
  10. E. Peli, “Adaptive Enhancement Based on a Visual Model,” Opt. Eng. 26, 655 (1987).
    [CrossRef]
  11. S. Mitra, B. S. Nutter, T. F. Krile, R. H. Brown, “Automated Method for Fundus Image Registration and Analysis,” Appl. Opt. 27, 1107 (1988).
    [CrossRef] [PubMed]
  12. Y. Tagami, “Correlations Between Atrophy of Maculo-Papillar Bundles and Visual Functions in Cases of Optic Neuropathies,” Doc. Ophthalmol. Proc. Ser. 19, 17 (1979).
    [CrossRef]
  13. M. Lundström, J-O Eklundh, “Computer Densitometry of Retinal Nerve Fibre Atrophy: a Pilot Study,” Acta Ophthalmol. 58, 639 (1980).
  14. The term densitometry is used here for measurements of reflectance gray levels rather than the common use for log(1/T), where T is the transmission fraction.
  15. The q value used here is equivalent to the p value commonly used to denote the confidence level in a difference between two measured variables.
  16. J. A. Swets, R. M. Pickett, Evaluation of Diagnostic Systems Methods from Signal Detection Theory (Academic, New York, 1982).
  17. H. A. Quigley, “Examination of the Retinal Nerve Fiber Layer in the Recognition of Early Glaucoma Damage,” Trans. Am. Ophthalmol. Soc. 84, 920 (1986).
    [PubMed]
  18. H. A. Quigley, E. M. Addicks, “Quantitative Studies of Retinal Nerve Fiber Layer Defects,” Arch. Ophthalmol. 100, 807 (1982).
    [CrossRef] [PubMed]
  19. R. S. Manor et al., “Narrow-Band (540-nm) Green-Light Stereoscopic Photography of the Surface Details of the Peripapillary Retina,” Am. J. Ophthalmol. 91, 774 (1981).
    [PubMed]
  20. T. Takamoto, B. Schwartz, “Photogrammetric Nerve Fiber Layer (NFL) Thickness Measurements in Normal, Ocular Hypertensive (OH), and Glaucomatous (OAG) Eyes,” Invest. Ophthalmol. Vis. Sci. 29(suppl), 421 (1988).
  21. A. Plesch, U. Klingbeil, J. Bille, “Digital Laser Scanning Fundus Camera,” Appl. Opt. 26, 1480 (1987).
    [CrossRef] [PubMed]
  22. R. H. Webb, G. W. Hughes, F. C. Delori, “Confocal Scanning Laser Ophthalmoscope,” Appl. Opt. 26, 1492 (1987).
    [CrossRef] [PubMed]

1988 (2)

T. Takamoto, B. Schwartz, “Photogrammetric Nerve Fiber Layer (NFL) Thickness Measurements in Normal, Ocular Hypertensive (OH), and Glaucomatous (OAG) Eyes,” Invest. Ophthalmol. Vis. Sci. 29(suppl), 421 (1988).

S. Mitra, B. S. Nutter, T. F. Krile, R. H. Brown, “Automated Method for Fundus Image Registration and Analysis,” Appl. Opt. 27, 1107 (1988).
[CrossRef] [PubMed]

1987 (4)

R. H. Webb, G. W. Hughes, F. C. Delori, “Confocal Scanning Laser Ophthalmoscope,” Appl. Opt. 26, 1492 (1987).
[CrossRef] [PubMed]

A. Plesch, U. Klingbeil, J. Bille, “Digital Laser Scanning Fundus Camera,” Appl. Opt. 26, 1480 (1987).
[CrossRef] [PubMed]

E. Peli, “Adaptive Enhancement Based on a Visual Model,” Opt. Eng. 26, 655 (1987).
[CrossRef]

E. Peli et al., “Nerve Fiber Layer Photography: a Comparative Study,” Acta Ophthalmol. 65, 71 (1987).

1986 (2)

E. Peli, T. R. Hedges, B. Schwartz, “Computerized Enhancement of Retinal Nerve Fiber Layer,” Acta Ophthalmol. 64, 113 (1986).

H. A. Quigley, “Examination of the Retinal Nerve Fiber Layer in the Recognition of Early Glaucoma Damage,” Trans. Am. Ophthalmol. Soc. 84, 920 (1986).
[PubMed]

1984 (2)

A. Sommer et al., “Cross-Polarization Photography of the Nerve Fiber Layer,” Arch. Ophthalmol. 102, 864 (1984).
[CrossRef] [PubMed]

A. Sommer et al., “Evaluation of Nerve Fiber Layer Assessment,” Arch. Ophthalmol. 102, 1766 (1984).
[CrossRef] [PubMed]

1983 (1)

A. Sommer, S. A. D’Anna, H. A. Kues, T. George, “High-Resolution Photography of the Retinal Nerve Fiber Layer,” Am. J. Ophthalmol. 96, 535 (1983).
[PubMed]

1982 (2)

P. J. Airaksinen, H. Nieminen, E. Mustonen, “Retinal Nerve Fiber Layer Photography with a Wide Angle Fundus Camera,” Acta Ophthalmol. 60, 362 (1982).

H. A. Quigley, E. M. Addicks, “Quantitative Studies of Retinal Nerve Fiber Layer Defects,” Arch. Ophthalmol. 100, 807 (1982).
[CrossRef] [PubMed]

1981 (1)

R. S. Manor et al., “Narrow-Band (540-nm) Green-Light Stereoscopic Photography of the Surface Details of the Peripapillary Retina,” Am. J. Ophthalmol. 91, 774 (1981).
[PubMed]

1980 (1)

M. Lundström, J-O Eklundh, “Computer Densitometry of Retinal Nerve Fibre Atrophy: a Pilot Study,” Acta Ophthalmol. 58, 639 (1980).

1979 (1)

Y. Tagami, “Correlations Between Atrophy of Maculo-Papillar Bundles and Visual Functions in Cases of Optic Neuropathies,” Doc. Ophthalmol. Proc. Ser. 19, 17 (1979).
[CrossRef]

1977 (1)

A. Vannas, C. Raitta, S. Lemberg, “Photography of the Nerve Fiber Layer in Retinal Disturbances,” Acta Ophthalmol. 55, 79 (1977).

1976 (1)

M. Lundström, L. Frisén, “Atrophy of Optic Nerve Fibres in Compression of the Chiasm; Degree and Distribution of Ophthalmoscopic Changes,” Acta Ophthalmol. 54, 623 (1976).

1973 (1)

W. F. Hoyt, L. Frisén, N. M. Newman, “Funduscopy of Nerve Fiber Layer Defects in Glaucoma,” Invest. Ophthalmol. 12, 814 (1973).
[PubMed]

Addicks, E. M.

H. A. Quigley, E. M. Addicks, “Quantitative Studies of Retinal Nerve Fiber Layer Defects,” Arch. Ophthalmol. 100, 807 (1982).
[CrossRef] [PubMed]

Airaksinen, P. J.

P. J. Airaksinen, H. Nieminen, E. Mustonen, “Retinal Nerve Fiber Layer Photography with a Wide Angle Fundus Camera,” Acta Ophthalmol. 60, 362 (1982).

Bille, J.

Brown, R. H.

D’Anna, S. A.

A. Sommer, S. A. D’Anna, H. A. Kues, T. George, “High-Resolution Photography of the Retinal Nerve Fiber Layer,” Am. J. Ophthalmol. 96, 535 (1983).
[PubMed]

Delori, F. C.

Eklundh, J-O

M. Lundström, J-O Eklundh, “Computer Densitometry of Retinal Nerve Fibre Atrophy: a Pilot Study,” Acta Ophthalmol. 58, 639 (1980).

Frisén, L.

M. Lundström, L. Frisén, “Atrophy of Optic Nerve Fibres in Compression of the Chiasm; Degree and Distribution of Ophthalmoscopic Changes,” Acta Ophthalmol. 54, 623 (1976).

W. F. Hoyt, L. Frisén, N. M. Newman, “Funduscopy of Nerve Fiber Layer Defects in Glaucoma,” Invest. Ophthalmol. 12, 814 (1973).
[PubMed]

George, T.

A. Sommer, S. A. D’Anna, H. A. Kues, T. George, “High-Resolution Photography of the Retinal Nerve Fiber Layer,” Am. J. Ophthalmol. 96, 535 (1983).
[PubMed]

Hedges, T. R.

E. Peli, T. R. Hedges, B. Schwartz, “Computerized Enhancement of Retinal Nerve Fiber Layer,” Acta Ophthalmol. 64, 113 (1986).

Hoyt, W. F.

W. F. Hoyt, L. Frisén, N. M. Newman, “Funduscopy of Nerve Fiber Layer Defects in Glaucoma,” Invest. Ophthalmol. 12, 814 (1973).
[PubMed]

Hughes, G. W.

Klingbeil, U.

Krile, T. F.

Kues, H. A.

A. Sommer, S. A. D’Anna, H. A. Kues, T. George, “High-Resolution Photography of the Retinal Nerve Fiber Layer,” Am. J. Ophthalmol. 96, 535 (1983).
[PubMed]

Lemberg, S.

A. Vannas, C. Raitta, S. Lemberg, “Photography of the Nerve Fiber Layer in Retinal Disturbances,” Acta Ophthalmol. 55, 79 (1977).

Lundström, M.

M. Lundström, J-O Eklundh, “Computer Densitometry of Retinal Nerve Fibre Atrophy: a Pilot Study,” Acta Ophthalmol. 58, 639 (1980).

M. Lundström, L. Frisén, “Atrophy of Optic Nerve Fibres in Compression of the Chiasm; Degree and Distribution of Ophthalmoscopic Changes,” Acta Ophthalmol. 54, 623 (1976).

Manor, R. S.

R. S. Manor et al., “Narrow-Band (540-nm) Green-Light Stereoscopic Photography of the Surface Details of the Peripapillary Retina,” Am. J. Ophthalmol. 91, 774 (1981).
[PubMed]

Mitra, S.

Mustonen, E.

P. J. Airaksinen, H. Nieminen, E. Mustonen, “Retinal Nerve Fiber Layer Photography with a Wide Angle Fundus Camera,” Acta Ophthalmol. 60, 362 (1982).

Newman, N. M.

W. F. Hoyt, L. Frisén, N. M. Newman, “Funduscopy of Nerve Fiber Layer Defects in Glaucoma,” Invest. Ophthalmol. 12, 814 (1973).
[PubMed]

Nieminen, H.

P. J. Airaksinen, H. Nieminen, E. Mustonen, “Retinal Nerve Fiber Layer Photography with a Wide Angle Fundus Camera,” Acta Ophthalmol. 60, 362 (1982).

Nutter, B. S.

Peli, E.

E. Peli, “Adaptive Enhancement Based on a Visual Model,” Opt. Eng. 26, 655 (1987).
[CrossRef]

E. Peli et al., “Nerve Fiber Layer Photography: a Comparative Study,” Acta Ophthalmol. 65, 71 (1987).

E. Peli, T. R. Hedges, B. Schwartz, “Computerized Enhancement of Retinal Nerve Fiber Layer,” Acta Ophthalmol. 64, 113 (1986).

Pickett, R. M.

J. A. Swets, R. M. Pickett, Evaluation of Diagnostic Systems Methods from Signal Detection Theory (Academic, New York, 1982).

Plesch, A.

Quigley, H. A.

H. A. Quigley, “Examination of the Retinal Nerve Fiber Layer in the Recognition of Early Glaucoma Damage,” Trans. Am. Ophthalmol. Soc. 84, 920 (1986).
[PubMed]

H. A. Quigley, E. M. Addicks, “Quantitative Studies of Retinal Nerve Fiber Layer Defects,” Arch. Ophthalmol. 100, 807 (1982).
[CrossRef] [PubMed]

Raitta, C.

A. Vannas, C. Raitta, S. Lemberg, “Photography of the Nerve Fiber Layer in Retinal Disturbances,” Acta Ophthalmol. 55, 79 (1977).

Schwartz, B.

T. Takamoto, B. Schwartz, “Photogrammetric Nerve Fiber Layer (NFL) Thickness Measurements in Normal, Ocular Hypertensive (OH), and Glaucomatous (OAG) Eyes,” Invest. Ophthalmol. Vis. Sci. 29(suppl), 421 (1988).

E. Peli, T. R. Hedges, B. Schwartz, “Computerized Enhancement of Retinal Nerve Fiber Layer,” Acta Ophthalmol. 64, 113 (1986).

Sommer, A.

A. Sommer et al., “Evaluation of Nerve Fiber Layer Assessment,” Arch. Ophthalmol. 102, 1766 (1984).
[CrossRef] [PubMed]

A. Sommer et al., “Cross-Polarization Photography of the Nerve Fiber Layer,” Arch. Ophthalmol. 102, 864 (1984).
[CrossRef] [PubMed]

A. Sommer, S. A. D’Anna, H. A. Kues, T. George, “High-Resolution Photography of the Retinal Nerve Fiber Layer,” Am. J. Ophthalmol. 96, 535 (1983).
[PubMed]

Swets, J. A.

J. A. Swets, R. M. Pickett, Evaluation of Diagnostic Systems Methods from Signal Detection Theory (Academic, New York, 1982).

Tagami, Y.

Y. Tagami, “Correlations Between Atrophy of Maculo-Papillar Bundles and Visual Functions in Cases of Optic Neuropathies,” Doc. Ophthalmol. Proc. Ser. 19, 17 (1979).
[CrossRef]

Takamoto, T.

T. Takamoto, B. Schwartz, “Photogrammetric Nerve Fiber Layer (NFL) Thickness Measurements in Normal, Ocular Hypertensive (OH), and Glaucomatous (OAG) Eyes,” Invest. Ophthalmol. Vis. Sci. 29(suppl), 421 (1988).

Vannas, A.

A. Vannas, C. Raitta, S. Lemberg, “Photography of the Nerve Fiber Layer in Retinal Disturbances,” Acta Ophthalmol. 55, 79 (1977).

Webb, R. H.

Acta Ophthalmol (2)

A. Vannas, C. Raitta, S. Lemberg, “Photography of the Nerve Fiber Layer in Retinal Disturbances,” Acta Ophthalmol. 55, 79 (1977).

M. Lundström, L. Frisén, “Atrophy of Optic Nerve Fibres in Compression of the Chiasm; Degree and Distribution of Ophthalmoscopic Changes,” Acta Ophthalmol. 54, 623 (1976).

Acta Ophthalmol. (4)

P. J. Airaksinen, H. Nieminen, E. Mustonen, “Retinal Nerve Fiber Layer Photography with a Wide Angle Fundus Camera,” Acta Ophthalmol. 60, 362 (1982).

E. Peli et al., “Nerve Fiber Layer Photography: a Comparative Study,” Acta Ophthalmol. 65, 71 (1987).

E. Peli, T. R. Hedges, B. Schwartz, “Computerized Enhancement of Retinal Nerve Fiber Layer,” Acta Ophthalmol. 64, 113 (1986).

M. Lundström, J-O Eklundh, “Computer Densitometry of Retinal Nerve Fibre Atrophy: a Pilot Study,” Acta Ophthalmol. 58, 639 (1980).

Am. J. Ophthalmol. (2)

A. Sommer, S. A. D’Anna, H. A. Kues, T. George, “High-Resolution Photography of the Retinal Nerve Fiber Layer,” Am. J. Ophthalmol. 96, 535 (1983).
[PubMed]

R. S. Manor et al., “Narrow-Band (540-nm) Green-Light Stereoscopic Photography of the Surface Details of the Peripapillary Retina,” Am. J. Ophthalmol. 91, 774 (1981).
[PubMed]

Appl. Opt. (3)

Arch. Ophthalmol. (3)

A. Sommer et al., “Cross-Polarization Photography of the Nerve Fiber Layer,” Arch. Ophthalmol. 102, 864 (1984).
[CrossRef] [PubMed]

A. Sommer et al., “Evaluation of Nerve Fiber Layer Assessment,” Arch. Ophthalmol. 102, 1766 (1984).
[CrossRef] [PubMed]

H. A. Quigley, E. M. Addicks, “Quantitative Studies of Retinal Nerve Fiber Layer Defects,” Arch. Ophthalmol. 100, 807 (1982).
[CrossRef] [PubMed]

Doc. Ophthalmol. Proc. Ser. (1)

Y. Tagami, “Correlations Between Atrophy of Maculo-Papillar Bundles and Visual Functions in Cases of Optic Neuropathies,” Doc. Ophthalmol. Proc. Ser. 19, 17 (1979).
[CrossRef]

Invest. Ophthalmol (1)

W. F. Hoyt, L. Frisén, N. M. Newman, “Funduscopy of Nerve Fiber Layer Defects in Glaucoma,” Invest. Ophthalmol. 12, 814 (1973).
[PubMed]

Invest. Ophthalmol. Vis. Sci. (1)

T. Takamoto, B. Schwartz, “Photogrammetric Nerve Fiber Layer (NFL) Thickness Measurements in Normal, Ocular Hypertensive (OH), and Glaucomatous (OAG) Eyes,” Invest. Ophthalmol. Vis. Sci. 29(suppl), 421 (1988).

Opt. Eng. (1)

E. Peli, “Adaptive Enhancement Based on a Visual Model,” Opt. Eng. 26, 655 (1987).
[CrossRef]

Trans. Am. Ophthalmol. Soc. (1)

H. A. Quigley, “Examination of the Retinal Nerve Fiber Layer in the Recognition of Early Glaucoma Damage,” Trans. Am. Ophthalmol. Soc. 84, 920 (1986).
[PubMed]

Other (3)

The term densitometry is used here for measurements of reflectance gray levels rather than the common use for log(1/T), where T is the transmission fraction.

The q value used here is equivalent to the p value commonly used to denote the confidence level in a difference between two measured variables.

J. A. Swets, R. M. Pickett, Evaluation of Diagnostic Systems Methods from Signal Detection Theory (Academic, New York, 1982).

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Figures (6)

Fig. 1
Fig. 1

Schematic presentation of the density averaging technique.(a) Schematic presentation of a retinal nerve fiber layer (RNFL) image with a wedge defect. The grey level information is sampled along lines perpendicular to the RNFL pattern (open arrows). The grey levels are averaged along lines parallel to the RNFL (dark arrows). (b) The average data from four curves generate one curve representing the grey levels across the RNFL (black in the image is represented by low level on the curve and white by high). This final, lowest curve is the averaged density curve used to evaluate the RNFL striations.

Fig. 2
Fig. 2

Illustration of the effect of cumulative averaged density. The bright line across the retinal nerve fiber layer striations represents the area from which the densitometry measures were taken. The curves on the right represent the cumulative averaged density. The lowest curve is the measurement from one line only, the second curve the average of two lines, the third the average of three lines, etc. Note that there are only minor changes in the curves after three averages. The numbers on the right represent diff(m) for the corresponding pair of averaged density curves.

Fig. 3
Fig. 3

Variability measurements illustrated for a normal retina. The rectangular area in the arcade represents the area from which measurements were taken. The density curves on the right are from measurements across the retinal nerve fiber layer (RNFL), and the curves on the left from measurements along the RNFL.

Fig. 4
Fig. 4

Illustration of the corrected variability measurements for normal retinal nerve fiber layer (RNFL). The dark curves represent the density measurements taken as in Fig. 3. The white curves represent the running average curve described in Eq. (6b). The variability is calculated from the difference between the white and dark curves. Note that the variability on the right (across the RNFL) is larger than that on the left (along the RNFL).

Fig. 5
Fig. 5

Comparison of variability measurement in an apparently normal and damaged retinal nerve fiber layer (RNFL) in the same eye of a patient with Leber’s optic atrophy. (a) Measurements taken outside the vascular arcade, normal RNFL. The density along the RNFL (bottom) and the density across the RNFL (top). Note that the high spatial frequency variability across the RNFL is larger, even at this measurement area, outside the arcade. The difference is even greater inside the arcade. (b) Measurement in the papillomacular bundle area of advanced diffused atrophy results in variability along which is similar to the variability across the RNFL. Note: the density curves in (a) and (b) are not to the same scale.

Fig. 6
Fig. 6

Correlation between the measured q values and the grading of the retinal nerve fiber layer by two trained observers. Although the observers have different biases, their coefficients of correlation are very similar and both are highly significant despite the apparent variability in the data.

Tables (1)

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Table I Measurements of Retinal Nerve Fiber Layer Striations in Diseased, Suspect, and Normal Eyes

Equations (9)

Equations on this page are rendered with MathJax. Learn more.

x i = ( x i , 1 , x i , 2 , x i ,   n ) .
X = ( x 1 , 1 , x 1 , 2 , x 1 , n x i , 1 , x m , 1 , x m , n )
X m = ( x 1 m , x 2 m , , x n m ) ,
x j m = 1 m i = 1 m x i , j .
d i f f ( m ) = j = 1 n ( x j m + 1 x j m ) .
var = 1 n 1 j = 1 n ( x j m x ) 2 ,
x = 1 n j = 1 n x j m
var k = 1 n 1 j = 1 n ( x j m x j k ) 2 ,
x j = k ∑  l = k + k ( 1 + cos π l k ) x j + l m ∑  l = k + k ( 1 + cos π l k )

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