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alents (SE). We first observed fundus changes in each patient using video files created from digital photographs using Adobe. Photoshop. 7.0Ò software (Adobe.
Acta Ophthalmologica 2008

Longterm findings in peripapillary crescent formation in eyes with mild or moderate myopia Mitsuru Nakazawa,1 Junji Kurotaki1,2 and Hiroshi Ruike2 1

Department of Ophthalmology, Hirosaki University Graduate School of Medicine, Hirosaki, Japan 2 Kurotaki Eye Clinic, Hachinohe, Japan

ABSTRACT. Purpose: To describe early changes of optic disc deviation and peripapillary crescent formation in eyes with mild or moderate myopia. Methods: We carried out a retrospective review of medical records and fundus photographs. We evaluated serial fundus photographs taken in 10 patients with mild or moderate myopia. We observed longterm changes in optic disc areas by creating video files using these photographs and Photoshop and Windows Movie Maker software. The distance between the fovea and the temporal edge of the optic disc was measured in each photograph and any gradual changes in distance between these in the same patient were regarded as representative of optic disc deviation. Correlations between optic disc deviation (0– 34.5% disc diameter) and either progression of myopia () 0.75 D to 6.25 D) or length of follow-up (21–98 months) were statistically examined. Results: On video files, the optic disc appeared to gradually deviate towards the nasal side and the myopic crescent developed gradually in the temporal side of the optic disc in most myopic patients. A significant correlation was found between optic disc deviation and progression of myopia (r2 = 0.61, p < 0.0001), but no correlation was detected between disc deviation and follow-up period (r2 = 0.055, p = 0.33). As optic disc deviation progressed, the peripapillary crescent became larger. Conclusions: The optic disc appears to deviate mostly nasally as myopia progresses and the peripapillary crescent forms as a result of optic disc deviation in eyes with mild or moderate myopia. Key words: conus – crescent – myopia – optic disc

Acta Ophthalmol. 2008: 86: 626–629 ª 2008 The Authors Journal compilation ª 2008 Acta Ophthalmol

doi: 10.1111/j.1600-0420.2007.01139.x

Introduction Formation of a peripapillary crescent is one of the characteristic features of optic disc changes in myopia. The mechanism of development for this structure has long been discussed. Duke-Elder & Abrams (1970) summa-

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rized four possible mechanisms for the formation of the myopic crescent: (1) scleral stretching which causes the choroid to be dragged back into scleral ectasia at the posterior pole; (2) excessive response of the sclera to stimulation of retinal growth;

(3) localized atrophy of the choroid in the peripapillary area, and (4) backward pull of the optic nerve, pull of the superior oblique muscle, or pull of the ciliary muscles in accommodation. Histological findings have shown complete or partial absence of the choroid in the area of the crescent and the termination of Bruch’s membrane with the choroid and retinal pigment epithelium (RPE) (Duke-Elder & Abrams 1970). Grossniklaus & Green (1992) performed a histopathological study of highly myopic eyes and Yasuzumi et al. (2003) reported the results of fluorescein and indocyanine green angiography in high myopia. Although these cross-sectional studies suggested scleral stretching as a mechanism for myopic fundus changes, they were performed using only eyes with pathological myopia. To understand the mechanisms behind myopic fundus changes, however, longterm observation of early and moderate changes in the same patients is essential. The present study therefore reviewed serial fundus photographs taken in 10 patients with mild or moderate myopia, and observed longterm changes in the peripapillary area, including the optic disc and surrounding tissues, as myopia progressed, using quantitatively analysed video files.

Materials and Methods We retrospectively reviewed fundus photographs taken periodically over a

Acta Ophthalmologica 2008

mean of 64 months (range 21– 98 months) in 10 Japanese patients (six women, four men) with mild or moderate myopia (± 0.00 D to ) 4.75 D). Informed consent for the use of fundus photographs was obtained from all patients. Mean age was 18.5 years (range 5–55 years). All patients were photographed using a digital fundus camera (TRC-NW3S, TRC-NW5SF or TRC-NW6S; Topcon Corp., Tokyo, Japan) at the same angle (45 degrees). Refraction was measured using an autorefractometer (KR-3100, KR-8100PA or KR-9000PW; Topcon Corp.) in all patients on the same day as fundus photography. Refractive data were expressed as spherical equivalents (SE). We first observed fundus changes in each patient using video files created from digital photographs using Adobe Photoshop 7.0 software (Adobe Systems Inc., San Jose, CA, USA) and Windows Movie maker (Microsoft Corp., Redmond, WA, USA). When each video file was made, the fovea centralis in each photograph was fixed as the central position. We then played the video files using Windows Media Player 1 (Microsoft Corp.). We vertically displayed three consecutive photographs (initial, intermediate and final) taken in the same patient (Figs 1–3) and measured the distance between the fovea centralis (a) and the temporal edge of the optic disc (b in the initial photograph and c in the final photograph). We then calculated the distance between the initial (b) and final (c) positions of the temporal edge of the optic disc. Optic disc deviation (%) was defined as the distance between b and c divided by the horizontal diameter of the optic disc (DD). We statistically analysed correlations between optic disc deviation (percentage of DD) and progression of myopia (DSE) in each patient, and between optic disc deviation and length of follow-up in each patient. Student’s t-test was employed for statistical examinations. When the peripapillary crescent was already present in the initial photograph, we drew a line (d) at the margin of the crescent (Fig. 2).

Results When we observed the video file of each patient, the optic disc appeared

b c

a b c a

(A)

(B)

Fig. 1. Nasal deviation of optic disc of patients 3 (A) and 4 (B) from position b to position c shown by initial (uppermost), intermediate (middle) and final (lowest) photographs. Numbers to the right of each photograph represent year (upper) and spherical equivalent (lower). (A) Right eye of patient 3. The vessel indicated by an arrow was initially outside the disc (1998) and moved into the disc area (2006). (B) Right eye of patient 4.

a

a

db c

(A)

db c

(B)

Fig. 2. Nasal deviation of the optic disc where the peripapillary crescent was already present on the initial photograph. Position d indicates the original location of the margin of the peripapillary crescent. (A) Right eye of patient 7. The vessel indicated by an arrow was originally located at the upper nasal margin (2001) and moved to the centre of the disc (2006). (B) Right eye of patient 10. The vascular loop indicated by an arrow was originally located in the central portion of the disc (1999) and moved relative to the temporal edge of the optic disc (2006).

a

bc

(A)

a

cb

d

(B)

Fig. 3. (A) Right eye of patient 6. An example of an optic disc showing little sign of deviation during follow-up. (B) Temporal deviation of the optic disc in the right eye of patient 8. The optic disc apparently moved in a temporal direction from 1997 to 2004, leaving a crescent on the nasal side.

to gradually move nasally during follow-up, particularly in patients 3, 4, 5, 7 and 10. The peripapillary crescent

formed and expanded along the optic disc deviation (Supplementary files 1 and 2). Optic disc deviation and

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Acta Ophthalmologica 2008

50

50

R2 = 0.61 (p < 0.0001)

R2 = 0.055 (p = 0.3265) Disc deviation (% DD)

Disc deviation (% DD)

crescent formation are demonstrated in Figs 1 and 2. In addition, the distance between the temporal margin of the crescent and the fovea centralis remained constant in these patients and the shape of the temporal margin of the crescent appeared to conform to the original margin of the optic disc (Figs 1 and 2). We then measured the extent of optic disc deviation on each photograph and performed further analysis, as described in Materials and Methods. Data for each patient are summarized in Table 1. A significant correlation was found between optic disc deviation and the progression of myopia (p < 0.0001, r2 = 0.61) (Fig. 4A), although no significant relationship was seen between optic disc deviation and length of followup (p = 0.33, r2 = 0.055) (Fig. 4B). Most patients with progressive myopia showed nasal deviation of the optic disc, resulting in formation of the temporal crescent (Figs 1 and 2). The optic disc did not appear to deviate in patients with no progression of myopia (Fig. 3A). Only one eye (OD of patient 8) showed a temporally deviated optic disc as myopia progressed, where the myopic crescent formed at the nasal side of the optic disc (Fig. 3B).

40 30 20 10

–2 (A)

0

2

4

6

1 ⁄ OD ⁄ F ⁄ 13 1 ⁄ OS ⁄ F ⁄ 13 2 ⁄ OD ⁄ F ⁄ 15 2 ⁄ OS ⁄ F ⁄ 15 3 ⁄ OD ⁄ M ⁄ 7 3 ⁄ OS ⁄ M ⁄ 7 4 ⁄ OD ⁄ M ⁄ 6 4 ⁄ OS ⁄ M ⁄ 6 5 ⁄ OD ⁄ F ⁄ 12 5 ⁄ OS ⁄ F ⁄ 12 6 ⁄ OD ⁄ M ⁄ 55 6 ⁄ OS ⁄ M ⁄ 55 7 ⁄ OD ⁄ F ⁄ 13 7 ⁄ OS ⁄ F ⁄ 13 8 ⁄ OD ⁄ F ⁄ 13 8 ⁄ OS ⁄ F ⁄ 13 9 ⁄ OD ⁄ M ⁄ 46 9 ⁄ OS ⁄ M ⁄ 46 10 ⁄ OD ⁄ F ⁄ 5 10 ⁄ OS ⁄ F ⁄ 5

55 55 84 62 53 21 57 78 98 77

Change of refraction (ΔSE)

10

(B)

40

60

80

100

Follow-up periods (weeks)

Fig. 4. (A) Relationship between optic disc deviation and change in spherical equivalent (SE), revealing a significant correlation (r2 = 0.61, p < 0.0001). (B) Relationship between optic disc deviation and length of follow-up. No correlation was identified (r2 = 0.055, p = 0.3265). DD = disc diameter.

Discussion Ophthalmoscopic changes associated with myopia include myopic configuration of optic disc, posterior staphyloma, vitreous degeneration, macular degeneration such as haemorrhage, Fuchs’ spot, lacquer cracks, chorioretinal atrophy (Curtin 1962; Grossniklaus & Green 1992; Yasuzumi et al. 2003) and peripapillary detachment in pathological myopia (Freund et al. 2003). Among these, myopic configuration of the optic disc is the most

Initial

Final

DSE

Disc deviation, %DD

) 1.50 ) 1.50 ) 3.00 ) 3.00 ) 2.75 ) 2.75 ±0.00 ±0.00 ) 4.00 ) 3.50 ) 0.25 ) 0.75 ) 4.75 ) 4.75 ) 2.00 ) 4.75 ) 0.75 ) 0.25 ) 1.50 ) 1.50

) 4.75 ) 4.75 ) 3.25 ) 3.25 ) 8.50 ) 8.00 ) 2.75 ) 2.75 ) 7.00 ) 5.75 ) 0.50 ) 1.00 ) 9.00 ) 8.25 ) 4.25 ) 8.25 ±0.00 ±0.00 ) 7.75 ) 7.25

3.25 3.25 0.25 0.25 5.75 5.25 2.75 2.75 3 3 0.25 0.25 4.25 3.5 2.75 3.5 )0.75 )0.25 6.25 5.75

7 7 9 8.9 34.5 25.9 22.6 16.1 17.2 17.2 0 0 40 14.2 22.7 0 0 0 26.9 30.8

SE = spherical equivalent; DSE = change in SE; DD = disc diameter; OD = right eye; OS = left eye; M = male; F = female.

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20

20

8

SE Follow-up (month)

30

0

0

Table 1. Summary of length of follow-up periods, refraction and optic disc deviation in all patients. Patient ⁄ eye ⁄ sex ⁄ age (year)

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common feature and is known in histopathological terms as a ‘tilted’ disc (Curtin 1962; Duke-Elder & Abrams 1970; Grossniklaus & Green 1992; Vongphant et al. 2002). Histopathologically, the appearance of a tilted disc suggests that the phenomenon results from scleral stretching as myopia progresses (Grossniklaus & Green 1992). Clinically, this configuration appears as a peripapillary crescent. This is also called b-peripapillary atrophy and may be related to the pathogenesis of glaucomatous optic nerve fibre damage (Jonas & Naumann 1989; Jonas et al. 1989, 1999). Called a ‘temporal crescent’, this usually occurs at the temporal side of the optic disc, although the crescent may appear nasally (Raab et al. 1981) or inferiorly (Curtin 1962). Although the pathogenesis of a temporal crescent has been unclear, histopathological findings of such crescents have been demonstrated as a lack of normal photoreceptors, RPE and choroid at the margin of the optic disc and stretched sclera underneath associated with widening of the subdural and subarachnoid spaces (Grossniklaus & Green 1992). More recently, Yasuzumi et al. (2003) studied the peripapillary crescent using fluorescein and indocyanine green angiography and observed two different areas in the peripapillary crescent of highly myopic eyes: a hyperfluorescent outer zone and a hypofluorescent inner zone. In addition, only the outer zone has been found to show significant enlargement during follow-up (Grossniklaus & Green 1992). These findings imply the

Acta Ophthalmologica 2008

possibility that the optic disc may be stretched and ⁄ or deviated as myopia progresses and that this phenomenon may be associated with formation of the myopic crescent. As all these previous cross-sectional studies were carried out in patients with highly progressed pathological myopia, longitudinal changes during the formation of the peripapillary crescent in the relatively early stages of myopia in the same patients also need to be investigated. As mild or moderate myopia is far more common than pathological myopia, information regarding those stages of myopia is valuable. We observed longterm changes in the optic disc and peripapillary area, occurring as myopia progressed, by using a video format. The video clearly demonstrated the movement of the optic disc and the gradual formation of the crescent. In addition, in order to analyse these phenomena more quantitatively, the present study reviewed serial fundus photographs from the same patients with mild or moderate myopia. Reproducibility and repeatability in the acquisition of these photographs were reasonably assured. In fact, the size of the optic disc remained consistent in different pictures of the same eye of the same patient. Of the 10 patients, eight were in the first and second decades of life (Table 1). As myopic patients in this age group do not usually show myopic fundus changes except for peripapillary crescent formation (Kobayashi et al. 2005), the fovea centralis was easily identified on fundus photographs. The myopic dioptic level may represent the quantitative level of myopia, as none of our patients showed pathological fundus changes or abnormal ocular media that might influence refraction. The present results indicate that the distance between the fovea centralis and optic disc gradually changes in proportion to the progression of myopia and that the temporal margin of the crescent always maintains the same distance from the fovea centralis and corresponds to the original configuration of the optic disc margin (Figs 1 and 2). As the fovea centralis can be regarded as the centre of the retina on the visual axis, this phenomenon indicates that the optic disc deviates nasally relative to the fovea centralis in most patients as myopia progresses (Fig. 4). The peripapillary

crescent appears to lack RPE and part of the choriocapillaris on angiography, even in the outer zone (Yasuzumi et al. 2003), and the temporal margin of the crescent always maintains the same distance from the fovea centralis and the same configuration corresponding to the optic disc shape. Consequently, the RPE and choroid cannot cover the space made after optic disc deviation, probably because the scleral stretching and peripapillary crescent formed as a result of optic disc deviation result in a simultaneous shortage of RPE and choroid. Nasal deviation of the optic disc can also be supported by the relative movement of blood vessels temporally to the optic disc (Figs 1A and 2). In one eye, the optic disc moved temporarily and a peripapillary crescent was formed on the nasal side (Fig 3B). Although this is an unusual case, the nasal crescent is reportedly seen less frequently in pathological myopia (Curtin, 1962) In such unusual cases, myopic scleral stretching may occur predominantly in a different portion of the midperipheral or peripheral sclera compared with most cases. Further studies need to clarify the mechanisms by which myopic fundus changes form as myopia progresses in patients with mild or moderate stages of myopia and investigate relationships between the formation of the peripapillary crescent and glaucoma. As the present study shows, creating video files from serial fundus photographs can allow us to understand kinetic changes in retinal lesions more easily than viewing photographs in clinical practice.

Supplementary Material The following supplementary material is available for this article: video clip S1; video clip S2; video clip S3; video clip S4, and video clip S5. This material is available online at: http://www.blackwell-synergy.com/ aos/10.111/j.1600-0420.2006.01139.x. Please note: Blackwell Publishing is not responsible for the content of the functionality of any supplementary materials supplied by the authors. Any queries (other than missing material) should be directed to the corresponding author for the article.

References Curtin BJ (1962): The pathogenesis of congenital myopia. A study of 66 cases. Arch Ophthalmol 69: 166–173. Duke-Elder S & Abrams D (1970): Changes at the optic disc. Pathological myopia. In: Duke-Elder S (ed.). System of Ophthalmology, Ophthalmic Optics and Refraction, Vol. V. London: Henry Kimpton 317– 321. Freund KB, Ciardella AP, Yannuzzi LA, Pece A, Goldbaum M, Kokame GT, Orlock D. (2003): Peripapillary detachment in pathologic myopia. Arch Ophthalmol 121: 197–204. Grossniklaus HE & Green WR (1992): Pathologic findings in pathologic myopia. Retina 12: 127–133. Jonas JB & Naumann GOH (1989): Peripapillary choroidal atrophy in normal and glaucoma eyes. II. Correlations. Invest Ophthalmol Vis Sci 30: 919–926. Jonas JB, Nguyen XN, Gusek GC, Naumann GOH (1989): Peripapillary chorioretinal atrophy in normal and glaucoma eyes. I. Morphometric data. Invest Ophthalmol Vis Sci 30: 908–918. Jonas JJ, Budde WM & Lang PJ (1999): Peripapillary atrophy in the chronic open-angle glaucomas. Graefes Arch Clin Exp Ophthalmol 237: 793–799. Kobayashi K, Ohno-Matsui K, Kojima A, Shimada N, Yasuzumi K, Yoshida T, Futagami S, Tokoro T et al. (2005): Fundus characteristics of high myopia in children. Jpn J Ophthalmol 49: 306–311. Raab MF, Garoon I & LaFranco FP (1981): Myopic macular degeneration. Int Ophthalmol Clin 21: 51–69. Vongphant J, Mitchell P & Wang JJ (2002): Population prevalence of tilted optic disc and the relationship of this sign to refractive error. Am J Ophthalmol 133: 679– 685. Yasuzumi Y, Ohno-Matsui K, Yoshida T, Kojima A, Shimada N, Futagami S, Tokoro T, Mochizuki M. (2003): Peripapillary crescent enlargement in highly myopic eyes evaluated by fluorescein and indocyanine angiography. Br J Ophthalmol 87: 1088–1090.

Received on March 29th, 2007. Accepted on October 23rd, 2007. Correspondence: Mitsuru Nakazawa MD, PhD Department of Ophthalmology Hirosaki University Graduate School of Medicine 5 Zaifu-cho Hirosaki 036-8562 Japan Tel: + 81 172 39 5094 Fax: + 81 172 37 5735 Email: [email protected]

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