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Clinical Characteristics of Posterior Staphyloma in Eyes with Pathologic Myopia
Clinical Characteristics of Posterior Staphyloma in Eyes with Pathologic Myopia HUANG WEI HSIANG, KYOKO OHNO-MATSUI, NORIAKI SHIMADA, KENGO HAYASHI, MUKA MORIYAMA, TAKESHI YOSHIDA, TAKASHI TOKORO, AND MANABU MOCHIZUKI ● PURPOSE:
To determine the morphologic features (grade and type) of posterior staphylomas and to analyze the relationship between the morphologic features and the incidence of myopic macular lesions. ● DESIGN: Observational case series. ● METHODS: Two hundred and nine eyes of 108 consecutive patients with high myopia were studied. The grade of staphylomas was determined from B-scan ultrasonographic images across the optic disk. The type of staphyloma was determined by binocular funduscopy and was classified according to the criteria of Curtin. The participants were divided into two groups: younger than 50 years and 50 years and older. The long-term morphologic progression of staphylomas was analyzed in nine patients who were followed up for more than 20 years. ● RESULTS: Ninety percent of 209 eyes had a staphyloma. The prevalence of staphylomas and more advanced grades of staphylomas (> grade 2) were significantly higher in the older than in the younger patients. The higher grades of staphylomas were associated with more severe myopic retinal degeneration. Type II staphyloma was the most prominent overall; however, in older subjects, the incidence of type II was decreased significantly, and that of type IX was increased significantly. The eyes with type IX staphyloma tended to have more severe myopic retinal degeneration than eyes with type II staphylomas. The long-term follow-up study demonstrated a progression from type II to type IX with increasing age. ● CONCLUSIONS: These results suggest that the morphologic features of staphylomas worsens as the patient ages. The progression from type II to type IX probably increases the mechanical tension on the macular area of highly myopic eyes, which then leads to myopic fundus lesions. (Am J Ophthalmol 2008;146:102–110. © 2008 by Elsevier Inc. All rights reserved.)
Supplemental Material available at AJO.com. Accepted for publication Mar 4, 2008. From the Department of Ophthalmology and Visual Science, Tokyo Medical and Dental University, Bunkyo-ku, Tokyo, Japan. Inquiries to Kyoko Ohno-Matsui, Department of Ophthalmology and Visual Science, Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku, Tokyo 113, Japan; e-mail: [email protected]
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©
2008 BY
P
ATHOLOGIC MYOPIA IS ONE OF THE MOST FREQUENT
causes of secondary visual disturbances worldwide.1– 4 The prevalence of pathologic myopia is known to be different among races, and it is more common in the adult Asian population, at approximately 9%,2 than the 2% in the mainly White population in the United States of America.3 In the Beijing Eye Study of 4,409 Chinese individuals who were 40 years of age and older, pathologic myopia was the second most frequent cause of low vision and blindness.4 A posterior staphyloma is a protrusion of the posterior shell of the eye globe that frequently is found in highly myopic eyes and is considered to be a hallmark lesion. The scleral shell of highly myopic eyes has increased elasticity and a tendency to expand gradually and to thin. The collagen fibers in these eyes are pathologic5,6; the fibers are smaller in diameter, appear histologically immature, and may have fewer cross-linkages than those in emmetropic eyes.7 The development of a posterior staphyloma is accompanied by a stretching of the posterior fundus, resulting in various kinds of myopic lesions, for example, chorioretinal atrophy, choroidal neovascularization (CNV), macular retinoschisis, and macular holes. It is known that highly myopic eyes with a posterior staphyloma have a higher probability of having visual disturbances.8 Despite the importance of posterior staphylomas in highly myopic eyes, there have been few comprehensive studies on the morphologic features of posterior staphylomas.9 The most detailed study of posterior staphyloma was probably that carried out by Curtin 30 years ago.9 From our observations of more than 1,500 patients in our high myopia clinic over a period of 34 years, we hypothesize that a posterior staphyloma is present in a high percentage of patients with high myopia, and the morphologic features of the staphyloma change with increasing age. To test this hypothesis, we recruited 209 highly myopic eyes (108 consecutive patients), and the prevalence and the morphologic features (grades and types) of the staphylomas were determined for patients of different ages. Also, the longitudinal changes in the morphologic features of the posterior staphyloma were determined in nine patients who were followed up for more than 20 years in our high myopia clinic. Finally, we analyzed the relationship between the morphologic features of posterior staphyloma and the presence of myopic retinal degeneration.
ELSEVIER INC. ALL
RIGHTS RESERVED.
0002-9394/08/$34.00 doi:10.1016/j.ajo.2008.03.010
FIGURE 1. Illustration showing the classification of types of posterior staphyloma by Curtin.9
METHODS TWO HUNDRED AND NINE EYES OF 108 CONSECUTIVE PA-
tients with high myopia, refractive error of ⫺8.0 diopters (D) or more, or axial length of 26.5 mm or more were recruited prospectively from the High Myopia Clinic of the Tokyo Medical and Dental University between July 8, 2005 and December 16, 2005. Three eyes of three of these patients were not included because reliable ultrasonography could not be obtained because of dense cataracts. In addition, two eyes of two patients were not included because the eyes were not highly myopic, and two eyes of two patients also were not studied because of a history of posterior segment surgery (retinal detachment surgery and vitrectomy). The evaluations included refraction, axial length measurements, best-corrected visual acuity, detailed fundus drawings using indirect stereoscopic ophthalmoscopy, fluorescein angiography (FA), color fundus photography, and B-scan and A-scan ultrasonography. Informed consent was obtained from all patients for the FA. The patients were divided into two groups according to their age: group 1 consisted of 88 eyes of 44 patients who were younger than 50 years, and group 2 included 121 eyes of 64 patients who were 50 years of age and older. The posterior staphylomas were classified into different types and different grades. The type of posterior staphyloma was determined by the location, size, and severity (Figure 1)9 and was classified by binocular stereoscopic ophthalmoscopy. The staphylomas were classified into 10 types: types I through V were primary staphylomas, and types IV through X were compound staphylomas (Figure 1).9 The grade of the posterior staphyloma was determined from the B-scan and A-scan ultrasonographic images based on the criteria of Steidl and Pruett.10 The staphylomas were graded from zero to four based on the depth of the staphyloma measured on A-scan and B-scan ultrasonographic images obtained by Ultrascan (Alcon Surgical, Inc, Fort Worth, Texas, USA). The depth of the staphyloma was measured on a horizontal B-scan image across the VOL. 146, NO. 1
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FIGURE 2. Ultrasonography image showing the measurement of the grade of posterior staphyloma. The distance between the optic nerve plane and the deepest portion of the staphyloma is measured in a horizontal section of a B-mode ultrasonogram.
optic nerve head as the distance from the inner surface of the optic nerve head to the deepest part of the staphyloma (Figure 2). To ensure that the B-scan passed through the deepest part of the staphyloma, B scans were performed until five well-defined images were obtain from each eye. Because the variance of the depth of the staphyloma of each eye was small, we selected the average distance from the optic nerve head to the deepest part of the staphyloma for the grading. An elongated eye with a smooth scleral contour was graded as zero. A grade 1 staphyloma had a depth of 2 mm or less, a grade 2 staphyloma had a depth of more than 2 mm but less than 4 mm, a grade 3 staphyloma had a depth of more than 4 mm but less than 6 mm, and a grade 4 staphyloma had a depth of more than 6 mm. The same examiners (B.W.H., K.O.-M., T.Y.) determined the type and grade of the staphyloma in all of the IN
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eyes in a masked manner. Assessments of the intergrader and intragrader showed that the reliability was very good. Among the 108 patients, there were 15 eyes of nine patients who were followed up for more than 20 years. In each patient, the type of staphyloma was determined by stereoscopic fundus observations by three or more ophthalmologists independently at the initial visit, and each patient was examined at least once yearly thereafter. For these nine patients, the medical records and fundus photographs were analyzed retrospectively, and the long-term changes of the staphyloma were determined. The relationship between the morphologic features of staphyloma and myopic retinal degeneration also was analyzed in all patients. The degree of myopic chorioretinal changes was categorized in each patient according to the criteria of Avila and associates.11 The myopic fundus changes (M) were graded on a scale of increasing severity from zero to five: grade M0, normal-appearing posterior pole; grade M1, choroidal pallor and tessellation; grade M2, choroidal pallor and tessellation, with posterior staphyloma; grade M3, choroidal pallor and tessellation, with posterior staphyloma and lacquer cracks; grade M4, choroidal pallor and tessellation, with posterior staphyloma, lacquer cracks, and focal areas of deep choroidal atrophy; and grade M5, posterior pole with large geographic areas of deep choroidal atrophy (so-called bare sclera). The presence of CNV was determined by indirect ophthalmoscopy and fluorescein fundus angiography. The optical coherence tomography (OCT) examinations were performed through a dilated pupil using a commercially available OCT ophthalmoscope (C7; NIDEK, Aichi, Japan). Ten or more horizontal and vertical OCT scans (approximately 7 mm in length) were recorded in the macular area of each patient. The OCT images were analyzed carefully for the presence of macular holes, macular retinoschisis, and retinal detachments. The significance of differences in the data was determined by Fisher exact probability tests and Mann–Whitney U tests. A P value of less than .05 was considered statistically significant. For patients who had two eyes involved, only the data from the right eye was used for the statistical analyses.
TABLE 1. Patients and Study Eye Characteristics in Different Age Groups
Characteristics
Age (yrs), mean (SD) 39.0 (9.2) Reractive error (D), ⫺13.0 (4.3) mean (SD) Axial length (mm), 28.9 (1.9) mean (SD) Grades of myopic degeneration 0 M0 17 M1 13 M2 34 M3 24 M4 0 M5 Choroidal 15 neovascularization
P value
66.0 (8.5) ⫺13.0 (6.0)
⬍.0001* n.s.
29.2 (1.8)
n.s.
0 4 9 36 48 24 28
● GRADE OF POSTERIOR STAPHYLOMAS: The distribution of the grades of posterior staphylomas is shown in Table 2. Overall, 90% of all patients had a posterior staphyloma, and a grade 1 staphyloma was the most prevalent staphyloma observed, followed by grade 2. In group 1, 71 eyes (80.7%) had evidence of a staphyloma, and the grade 1 staphyloma was found in 64 eyes (72.7%) of the eyes. In group 1, staphylomas classified as grade 3 of higher were not detected. In group 2, 117 eyes (96.7%) of the eyes had a staphyloma, and the prevalence of a posterior staphyloma was significantly higher in group 2 than in group 1 (P ⫽ .0002). The prevalence of grade 1 was significantly lower in group 2 (45.5%) than in group 1 (72.7%). However, the prevalence of grade 2 was higher in group 2 (at 31.4%) than in group 1. In addition, the deeper staphylomas (grades 3 and 4) were found only in group 2. The differences in the prevalence of grade 1 and grade 2 staphylomas between groups 1 and 2 were statistically significant (P ⫽ .0001 and P ⬍ .0001, respectively). The axial lengths of eyes classified with grade 0 staphylomas were significantly shorter than all eyes with a staphyloma in both groups. However, the differences in the axial length between eyes with grades 1 and 2 and between grades 1 and 3 were not significant.
THE CHARACTERISTICS OF THE 108 PATIENTS (209 EYES) ARE
summarized in Table 1. There were 34 men and 74 women with a mean age of 55.0 ⫾ 14.9 years and a range of 23 to 78 years. The mean refractive error (spherical equivalent) was ⫺13.0 ⫾ 5.5 D, with a range ⫺8.5 to ⫺26.0 D, and the mean axial length was 29.3 ⫾ 1.9 mm, with a range of 26.5 to 33.0 mm. The differences in the refractive error and axial length between two groups were not significant. AMERICAN JOURNAL
Group 2 (ⱖ 50 yrs)
D ⫽ diopters; n.s. ⫽ not significant; SD ⫽ standard deviation. *Mann–Whitney U test.
RESULTS
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Group 1 (⬍ 50 yrs)
● TYPES OF POSTERIOR STAPHYLOMA:
The distribution of the different types of posterior staphyloma is summarized in Table 3. Types IV, VI, VII, VIII, and X were not observed in any of the eyes. The type II staphyloma was the most prevalent in both groups: 67.6% in group 1 and 43.6% in group 2. However, the prevalence of type II
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TABLE 2. Grades of Posterior Staphyloma and Axial Length in Different Age Groups Total
Group 1 (⬍50 yrs)
Group 2 (ⱖ 50 yrs)
Grades
No. (%)
Axial Length (mm)
No. (%)
Axial Length (mm)
No. (%)
Axial Length (mm)
0 1 2 3 4
21 eyes (10.0) 119 eyes (56.9) 45 eyes (21.5) 23 eyes (11.0) One eye (0.5)
27.0 ⫾ 1.13 29.0 ⫾ 1.68 29.9 ⫾ 1.57 29.7 ⫾ 1.28 31.3
17 eyes (19.3) 64 eyes (72.7) Seven eyes (8.0) 0 0
27.2 ⫾ 1.19 29.0 ⫾ 1.73 30.3 ⫾ 0.99 — —
4 eyes (3.3) 55 eyes (45.5) 38 eyes (31.4) 23 eyes (26.1) One eye (0.8)
26.5 ⫾ 0.39 29.1 ⫾ 1.61 29.8 ⫾ 1.66 29.7 ⫾ 1.28 31.3
The prevalence of grade 2 staphyloma was significantly higher in patients older than 50 years than in those younger than 50 years.
TABLE 3. Types of Posterior Staphyloma and Axial Length in Different Age Groups Total
Group 1 (⬍ 50 yrs)
Group 2 (ⱖ 50 yrs)
Types
No. (%)
Axial Length (mm)
No. (%)
Axial Length (mm)
No. (%)
Axial Length (mm)
I II III IV V VI VII VIII IX X
44 eyes (23.4) 99 eyes (52.7) 8 eyes (4.3) 0 5 eyes (2.7) 0 0 0 32 eyes (17.0) 0
29.1 ⫾ 1.92 29.2 ⫾ 1.64 27.5 ⫾ 1.20 — 29.1 ⫾ 0.18 — — — 30.1 ⫾ 1.63 —
13 eyes (18.3) 48 eyes (67.6) 6 eyes (8.5) 0 3 eyes (4.2) 0 0 0 1 eye (1.4) 0
28.8 ⫾ 1.54 29.4 ⫾ 1.21 26.9 ⫾ 0.71 — 28.9 ⫾ 0.23 — — — 30.5 —
31 eyes (26.5) 51 eyes (43.6) 2 eyes (1.7) 0 2 eyes (1.7) 0 0 0 31 eyes (26.5) 0
29.3 ⫾ 2.08 29.0 ⫾ 1.54 29.6 ⫾ 0.44 — 29.3 ⫾ 0.15 — — — 30.3 ⫾ 1.62 —
staphyloma was significantly higher in group 1 than in group 2 (P ⫽ .009). The major difference between the two groups was an increase in the prevalence of type IX staphyloma in group 2. A type IX staphyloma was seen in only one eye (1.4%) of group 1, but in 31 eyes (26.5%) in group 2 (P ⬍ .0001). In type IX staphylomas, a vertical septum with a width of one to two disk diameters was observed to pass from the upper to the lower border of the staphyloma (Figure 1).9 In all patients in group 1, the axial length of eyes with type III staphylomas was significantly shorter than that of eyes with each of the other types of staphylomas. In addition, the differences in the axial length between eyes with types I, II, and V staphylomas in all patients as well as between groups 1 and 2 were not significant. In group 2, the axial length of eyes with type IX staphylomas was significantly longer than eyes with types I and II staphylomas (P ⫽ .03 and .007, respectively). ● MYOPIC FUNDUS LESIONS AND GRADES OR TYPES OF POSTERIOR STAPHYLOMA: Eyes classified as M1, M2,
and M3, were categorized as having mild myopic retinal degeneration, and eyes classified as M4 and M5 were grouped as having severe myopic degeneration (Table 1). In group 1, 24 (27.3%) of 88 eyes had severe myopic degeneration, and in group 2, 71 (58.7%) of 121 eyes had severe myopic degeneration (Table 1). This difference was VOL. 146, NO. 1
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statistically significant (P ⬍ .0001). CNV was detected in 15 eyes (17.0%) in group 1 and in 28 eyes (23.1%) in group 2. This difference was not statistically significant. The relationships between myopic fundus lesions and the grade of the posterior staphyloma are summarized in Figure 3 and Table 4. Overall, our data showed that the higher the grade of the posterior staphyloma, the more severe the retinal degeneration tended to be (Figure 3). None of the eyes with grade 0 staphyloma had severe degeneration (M4 and M5), but 42.8% with grade 1 staphyloma had severe degeneration, 62.2% with grade 2 staphyloma had severe degeneration, 69.6% with grade 3 staphyloma had severe degeneration, and 100% with grade 4 staphyloma had severe degeneration. Although there was an increase in the prevalence of severe degeneration with an increase in the depth of the staphyloma, the differences among grades 1, 2, and 3 did not reach statistical significance. Because the patient age also may affect the grade of the myopic degeneration, we examined the grades of myopic degeneration in group 1 and in group 2 separately. The results demonstrated that even in older patients (group 2), the higher grades of posterior staphyloma were related to the development of more severe retinopathy (see Supplemental Tables 1 and 2 at AJO.com). A CNV was detected in 43 eyes (20.6%), lacquer cracks in 44 eyes (21.1%), macular retinoschisis in 24 eyes (11.5%), and macular holes in six eyes (2.9%) among all of IN
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excluded types III and V from the statistical analyses because the macular area was not included within the staphylomatous area in these two types. The prevalence of CNVs, active CNVs, and macular retinoschisis were not significantly different among eyes classified as types I, II, and IX staphylomas. However, eyes with lacquer cracks were detected significantly more frequently in eyes with type IX compared with type I staphyloma (P ⫽ .03) as well as with type II staphylomas (P ⬍ .001). ● LONG-TERM CHANGES IN POSTERIOR STAPHYLOMAS:
Fifteen eyes of nine patients were followed up for more than 20 years in our high myopia clinic. The clinical data of these nine patients are summarized in Table 6. The type of posterior staphyloma was determined by binocular indirect ophthalmoscopy at each follow-up examination by three or more ophthalmologists. At the initial examination, a posterior staphyloma was detected in 10 of 15 eyes, and all were classified as type II. Three eyes of three patients showed a change from type II to type IX staphyloma at 17 years (Case 1 in Table 6), 15 years (Case 2 in Table 6), and 18 years (Case 3 in Table 6) after the initial examination (Figure 5). In these patients, a ridge-like protrusion developed temporal to the optic disk at ages between their late 40s through the early 50s and transformed the staphyloma to type IX. In these three eyes that showed the progression of the type of staphyloma, a progression of myopic degeneration also was observed (Table 6). In contrast, in the other 12 eyes that did not show a change of the type of the posterior staphyloma, only two eyes showed a progression of myopic retinal degeneration.
FIGURE 3. Bar graph demonstrating the frequency of different grades of myopic degeneration as a function of the different grades of posterior staphyloma. The data showed that the higher the grade of the posterior staphyloma, the more severe the myopic retinal degeneration tended to be.
the 209 eyes. None of these types of lesion, that is, CNV, lacquer cracks, macular retinoschisis, and macular holes, was detected in eyes with grade 0 staphyloma. A CNV was detected in approximately 20% of the patients with grade 1 to 3 staphyloma, although the prevalence of CNVs was not significantly different among grades 1 to 3. Even when we examined the prevalence of the active phase of CNV only, there was no significant difference in the prevalence of active CNV among grades 1 to 3. The prevalence of lacquer cracks tended to increase as the grade of the staphyloma increased from grade 1 to 3, although the differences were not significant. Statistical analysis showed that macular retinoschisis was present significantly more frequently in eyes with grade 3 staphyloma than in eyes with grade 1 (P ⫽ .03). Macular holes were detected in only one to three eyes among grades 1 to 3. The distribution of the myopic fundus lesions and the types of posterior staphyloma is shown in Figure 4 and Table 5. Fifty percent of the eyes with type I staphyloma had severe retinal degeneration, 46.5% of eyes with type II staphyloma had severe degeneration, 50% of eyes with type III staphyloma had severe degeneration, none of the eyes with type V staphyloma had severe degeneration, and 71.9% of the eyes with type IX staphyloma had severe degeneration. Statistical analysis demonstrated that the eyes with type IX staphyloma had significantly more severe myopic retinal degeneration than those with type II staphyloma (P ⫽ .01). However, the difference in the prevalence of severe myopic retinal degeneration in eyes with type I and type IX staphylomas was not significant. The prevalence of severe myopic retinal degeneration in eyes with type I and type II staphyloma was significantly lower than in eyes with type IX staphyloma (P ⫽ .02). We 106
AMERICAN JOURNAL
DISCUSSION OUR RESULTS SHOWED THAT A STAPHYLOMA WAS PRESENT
in 90% of the patients with high myopia, and the prevalence of staphylomas was significantly higher in older patients (96.7% in those 50 years of age and older) than in younger patients (80.7% in patients younger than 50 years). Stiedl and Pruett10 reported that 88 (75.9%) of 116 eyes had a posterior staphyloma; however, they analyzed eyes with myopia ranging from ⫺3 to ⫺38 D with a mean of ⫺14 D. Thus, it is difficult to compare the prevalence of posterior staphylomas between the two studies, because the definition of myopia was different. The prevalence of grade 2 staphyloma was significantly higher in patients older than 50 years than in those younger than 50 years. This indicates that not only the incidence of posterior staphyloma but also the depth of the staphyloma increased as the patient ages. Interestingly, the axial length was not significantly different between eyes with grade 1 to 3 staphyloma. However, if we follow the changes in the grade of staphyloma in the same patient, it may be expected that the axial length would OF
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TABLE 4. The Relationship between Myopic Fundus Lesions and Grade of Posterior Staphyloma Variables
Choroidal neovascularization Choroidal neovascularization (active phase) Lacquer cracks Macular retinoschisis Macular holes Grades of myopic degeneration M0 M1 M2 M3 M4 M5
Grade 0 (21 Eyes)
Grade 1 (119 Eyes)
Grade 2 (45 Eyes)
Grade 3 (23 Eyes)
Grade 4 (One Eye)
0 eyes (0%)
27 eyes (22.7%)
11 eyes (24.4%)
Five eyes (21.7%)
0 eye (0%)
0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%)
Six eyes (5.0%) 23 eyes (19.3%) 11 eyes (9.2%) One eye (0.8%)
Two eyes (4.4%) 13 eyes (28.9%) Seven eyes (15.6%) Three eyes (6.7%)
One eye (4.3%) Eight eyes (34.8%) Six eyes (26.1%) Two eyes (8.7%)
0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%)
0 eyes (0%) 0 eyes (0%) 19 eyes (16.0%) 49 eyes (41.2%) 43 eyes (36.1%) Eight eyes (6.7%)
0 eyes (0%) 0 eyes (0%) Three eyes (6.7%) 14 eyes (31.1%) 17 eyes (37.8%) 11 eyes (24.4%)
0 eyes (0%) 0 eyes (0%) 0 eyes (0%) Seven eyes (30.4%) 12 eyes (52.2%) Four eyes (17.4%)
0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%) One eye (100%)
0 eyes (0%) 21 eyes (100%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%)
The data showed that the higher the grade of the posterior staphyloma, the more severe the retinal degeneration tended to be.
FIGURE 4. Bar graph demonstrating the frequency of different grades of myopic degeneration as a function of the different types of posterior staphyloma. The data showed that the frequency of the grade of myopic degeneration varied among the different types of staphylomas; however, eyes with type IX staphyloma had more severe myopic retinal degeneration than those with type II staphyloma.
increase with an increase in the grade of staphyloma. However, this was not found, probably because there was a wide range of axial lengths in eyes with a staphyloma at the initial examination. Curtin also reported an unusually wide range of refractive errors and axial lengths for eyes with the same type of staphyloma.9 The type II staphylomas were the most prominent type in groups 1 and 2. In contrast, Curtin reported that type I was the most prominent and was observed in 55% of the eyes with a posterior staphyloma, and the type II was observed in only 8.4% of the eyes examined (calculated from his Table II).9 Oie and associates examined the types VOL. 146, NO. 1
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of staphyloma in 28 Japanese with highly myopic eyes with a macular hole retinal detachment (MHRD) and in 47 highly myopic eyes without an MHRD.12 They reported that in the eyes with an MHRD, 19% had type I staphyloma and 63% had type II staphyloma, whereas in the group without an MHRD, 43% had type I staphyloma and 25% had type II staphyloma. Although the number of their patients was much smaller, their results also indicated that the prevalence of type II staphyloma was higher in Japanese patients than that reported by Curtin (who mainly studied White persons).9 In group 2, the prevalence of type II staphylomas was lower than in group 1, and instead, type IX staphyloma increased. In type IX staphyloma, a ridge-like protrusion was present temporal to the optic disk. And more importantly, in the patients who were followed up for more than 20 years, the ridge-like protrusion developed in the three patients who demonstrated the progression from type II to type IX staphyloma. These findings suggest that type IX staphylomas develop secondarily by the development of a ridge-like protrusion temporal to the optic disk in eyes originally with type II staphyloma as the patient ages. Therefore, our results indicated that the posterior staphyloma not only deepens, but its morphologic features also change as the patients grow older. This is important because these morphologic changes of the posterior staphyloma enhance the development of severe myopic retinal degeneration. The sclera is a typical connective tissue and consists of interwoven collagen fibrils in close association with proteoglycans. The number, arrangement, and types of collagen fibrils are considered to determine the mechanical strength of a sclera. The reason why the morphologic features of posterior staphyloma worsen with increasing age has not been clarified fully, and some authors have reported alterations in the composition of the sclera extracellular matrix in humans13,14 as well as animals.15 IN
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TABLE 5. The Relationship between Myopic Fundus Lesions and Type of Posterior Staphyloma Variables
Type I (44 Eyes)
Type II (99 Eyes)
Type III (8 Eyes)
Choroidal neovascularization Choroidal neovascularization (active phase) Lacquer cracks Macular retinoschisis Macular holes Grades of myopic degeneration M0 M1 M2 M3 M4 M5
Seven eyes (15.9%)
23 eyes (23.2%)
Two eyes (4.5%) 11 eyes (25%) Nine eyes (20.5%) Two eyes (4.5%) 0 eyes (0%) 0 eyes (0%) Two eyes (4.5%) 20 eyes (45.5%) 10 eyes (22.7%) 12 eyes (27.3%)
Type V (5 Eyes)
Type IX (32 Eyes)
Three eyes (37.5%)
0 eyes (0%)
10 eyes (31.3%)
Five eyes (5.1%) 17 eyes (17.2%) Nine eyes (9.1%) Two eyes (2.0%)
0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%)
0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%)
Two eyes (6.3%) 16 eyes (50%) Six eyes (18.8%) Two eyes (6.3%)
0 eyes (0%) 0 eyes (0%) 15 eyes (15.2%) 38 eyes (38.4%) 38 eyes (38.4%) Eight eyes (8.1%)
0 eyes (0%) 0 eyes (0%) Three eyes (37.5%) One eyes (12.5%) Four eyes (50%) 0 eyes (0%)
0 eyes (0%) 0 eyes (0%) One eyes (20%) Four eyes (80%) 0 eyes (0%) 0 eyes (0%)
0 eyes (0%) 0 eyes (0%) Two eyes (6.3%) Seven eyes (21.9%) 19 eyes (59.4%) Four eyes (12.5%)
TABLE 6. Characteristics of Patients with Long-Term Follow-up and the Long-Term Change of the Type of Posterior Staphyloma At Initial Examination Patient Age Refractive Axial Length Type of Myopic Age No. Sex Eye (yrs) Error (D) (mm) Staphyloma Degeneration* (yrs)
1 2
F F
3 4 5
F F F
6
F
7
M
8
F
9
M
R R L R L R L R L R L R L R L
42 48 47 48 44 29 50 35 35
⫺22.0 ⫺20.0 ⫺13.0 ⫺9.0 ⫺13.0 ⫺19.0 ⫺15.0 ⫺14.0 ⫺16.0 ⫺14.0 ⫺12.0 ⫺11.0 ⫺12.0 ⫺23.0 ⫺11.0
31.9 31.8 29.0 27.8 29.0 28.4 27.9 28.8 29.3 27.2 27.0 29.7 29.9 30.9 29.1
II II II II II II II II II 0 0 0 0 II 0
M4 M3 M3 M2 M3 M3 M3 M3 M3 M1 M1 M1 M1 M2 M1
68 70 74 70 66 49 70 58 58
Refractive Error (D)
⫺8.0 (IOL) ⫺6.0 (IOL) ⫺5.0 (IOL) ⫺4.25 (IOL) ⫺5.0 (IOL) ⫺19.0 ⫺15.0 ⫺18.0 ⫺18.0 ⫺15.0 ⫺15.0 ⫺11.0 ⫺12.5 ⫺23.0 ⫺11.5
At Final Examination Change of Axial Length Type of Myopic Type of Follow-up (mm) Staphyloma Degeneration* Staphyloma (yrs)
33.3 32.4 29.8 28.6 29.8 29.7 29.3 29.9 29.5 28.0 27.6 30.6 30.8 33.8 29.4
IX IX II IX II II II II II 0 0 0 0 II 0
M5 M4 M3 M3 M3 M4 M3 M3 M3 M1 M1 M1 M1 M3 M1
Y Y N Y N N N N N N N N N N N
26 22 27 22 22 29 20 23 23
D ⫽ diopter; F ⫽ female; IOL ⫽ intraocular lens; L ⫽ left; M ⫽ male; N ⫽ no; R ⫽ right; Y ⫽ yes. *See Methods for classification.
opment of macular retinoschisis. Although the mechanism of macular retinoschisis development has not been clarified fully, some causative factors such as the presence of vascular microfolds,18 paravascular inner lamellar hole,19 and subsequent tractional detachment of inner limiting membrane20 have been suggested. An increased mechanical tension caused by an increased depth of posterior staphyloma may facilitate these proposed causative factors. Stiedl and Pruett10 reported that the eyes with the shallowest staphyloma (grade 1) had the highest frequency of CNV. They suggested that it is possible that the grade 1 eyes may be healthier and more metabolically active with well-perfused chorioretinal tissue and good capacity to respond to injury by neovascular ingrowth. In contrast, the
Our results showed that the higher grades of staphyloma were associated with more severe myopic retinal degeneration, which was similar to the results previously reported by Stiedl and Pruett.10 Curtin and Karlin also reported a strong correlation between axial length and myopic chorioretinal atrophy, although the correlation between the myopic chorioretinopathy and posterior staphyloma was not reported.16 Among the independent myopic macular lesions, the prevalence of macular retinoschisis was significantly higher in eyes with grade 3 staphylomas compared with those with grade 1 staphylomas. We have reported that macular retinoschisis was detected only in highly myopic eyes with a posterior staphyloma,17 which supports the idea on the importance of staphylomas in the devel108
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FIGURE 5. Fundus photographs showing the progression from type II to type IX staphyloma (right fundus of Case 1 in Table 6). (Left) Right fundus of a 42-year-old woman. Refractive error was ⴚ22.0 diopters and the axial length was 31.9 mm. Type II staphyloma is visible (arrowheads), and the posterior fundus shows fibrovascular tissue (arrow) and focal chorioretinal atrophy. (Right) Twenty-six years later, the axial length of the same eye was 33.3 mm. A ridge-like protrusion can be seen temporal to the optic disk (arrows), and the type of staphyloma has progressed to type IX. Focal chorioretinal atrophy has spread widely and the posterior fundus shows a bare sclera appearance. The optic disk also is stretched vertically.
prevalence of CNV (total CNV and active CNV) was not different among different grades of staphylomas in our study. The reason for this discrepancy is not clear; however, one reason may be a difference in the classification of high myopia (⬎ ⫺3.0 D vs ⬎ ⫺8.0 D). Thus, it is possible that some of the CNVs in their study may have been nonmyopic in origin (e.g., idiopathic CNV). Our results showed that eyes with type IX staphylomas had severe myopic retinal degeneration more frequently than eyes with type II staphylomas (Table 5). In addition, the axial length of eyes with type IX staphyloma was significantly longer than those with type II staphyloma. We suggest that there is an increase in the mechanical tension on the posterior pole as well as on the optic disk by the ridge-like protrusion in eyes of type IX staphyloma and that this probably facilitates the development and progression of myopic retinal degeneration. The prevalence of lacquer cracks was significantly higher in eyes with type IX staphyloma than in those with type II staphyloma. Lacquer cracks are mechanical ruptures of the Bruch membrane caused by an axial elongation; therefore, an increased prevalence of lacquer cracks in eyes with type IX may reflect an increased mechanical expansion of the posterior fundus. One of the most interesting aspect of our study was that we were able to examine the morphologic features of the posterior staphyloma in 15 eyes of nine patients periodically for more than 20 years. The results showed the clear
progression from type II to type IX staphyloma in three patients. Our longitudinal study showed that all three of the eyes that showed a progression from type II to type IX staphyloma had a progression of myopic retinal degeneration, whereas only two of 12 eyes without the progression of the staphyloma showed a progression of the retinal degeneration. These findings indicate that the morphologic changes of the posterior staphyloma may be more important for the development or progression of myopic retinal degeneration than the axial length alone. In conclusion, we examined the grades and types of posterior staphyloma in a large number of Japanese patients with pathologic myopia. The results demonstrated that the type II staphyloma was the most prominent type in Japanese patients with high myopia. The grade of staphyloma and prevalence of type IX staphyloma was higher in older patients. These findings suggest that the posterior staphyloma not only deepens but also its morphologic features change as the patients age, even though the axial length does not change significantly. The longitudinal study revealed a clear progression from type II to type IX staphyloma in three of 15 patients. The progression to type IX staphyloma may be an important feature and may increase the mechanical tension on the macular area and optic disk, which may cause the progression to severe myopic retinal degeneration.
THIS STUDY WAS SUPPORTED IN PART BY RESEARCH GRANTS 16390495, 17591823, AND 19390441 FROM THE JAPAN SOCIETY FOR the Promotion of Science, Tokyo, Japan. The authors indicate no financial conflict of interest. Involved in design of study (H.W.H., K.O.-M.); conduct of study (H.W.H., K.O.-M., N.S., K.H., M.M., T.Y.); analysis and interpretation (H.W.H., N.S., K.H., M.M.); writing the article (H.W.H., K.O.-M.); critical revision of the article (K.O.-M., M.M., T.Y., T.T., M.M.); obtaining funding (K.O.-M., M.M.); literature search (H.W.H., K.O.-M., N.S., K.H.); and data collection (H.W.H., K.O.-M., N.S., K.H., M.M., T.Y.); review and approval of manuscript (K.O.M., T.T., M.M.) . Because the ultrasonography
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to measure the axial length and to evaluate the morphologic features of posterior staphyloma is performed routinely for highly myopic patients, the Institutional Review Board of the Tokyo Medical and Dental University determined that no approval to perform the examination is necessary. The procedures used conformed to the tenets of the Declaration of Helsinki. The authors thank Professor Duco Hamasaki, Bascom Palmer Eye Institute, Miami, Florida for his critical discussion in the early phase of this study and for the revision of the final manuscript.
12. Oie Y, Ikuno Y, Fujikado T, Tano Y. Relation of posterior staphyloma in highly myopic eyes with macular hole and retinal detachment. Jpn J Ophthalmol 2005;49:530 – 532. 13. Dunlevy JR, Summers Rada JA. Interaction of lumican with aggrecan in the aging human sclera. Invest Ophthalmol Vis Sci 2004;45:3849 –3856. 14. Rada JA, Achen VR, Penugonda S, Schmidt RW, Mount BA. Proteoglycan composition in the human sclera during growth and aging. Invest Ophthalmol Vis Sci 2000;41:1639 – 1648. 15. Albon J, Farrant S, Akhtar S, et al. Connective tissue structure of the tree shrew optic nerve and associated aging changes. Invest Ophthalmol Vis Sci 2007;48:2134 –2144. 16. Curtin BJ, Karlin DB. Axial length measurements and fundus changes of the myopic eye. Am J Ophthalmol 1971;71: 42–53. 17. Baba T, Ohno-Matsui K, Futagami S, et al. Prevalence and characteristics of foveal retinal detachment without macular hole in high myopia. Am J Ophthalmol 2003;135:338 –342. 18. Sayanagi K, Ikuno Y, Gomi F, Tano Y. Retinal vascular microfolds in highly myopic eyes. Am J Ophthalmol 2005; 139:658 – 663. 19. Shimada N, Ohno-Matsui K, Nishimuta A, et al. Detection of paravascular lamellar holes and other paravascular abnormalities by optical coherence tomography in eyes with high myopia. Ophthalmology 2008;115:708 –717. 20. Sayanagi K, Ikuno Y, Tano Y. Tractional internal limiting membrane detachment in highly myopic eyes. Am J Ophthalmol 2006;142:850 – 852.
REFERENCES 1. Ghafour IM, Allan D, Foulds WS. Common causes of blindness and visual handicap in the west of Scotland. Br J Ophthalmol 1983;67:209 –213. 2. Wong TY, Foster PJ, Hee J, et al. Prevalence and risk factors for refractive errors in adult Chinese in Singapore. Invest Ophthalmol Vis Sci 2000;41:2486 –2494. 3. Sperduto RD, Seigel D, Roberts J, et al. Prevalence of myopia in the United States. Arch Ophthalmol 1983;101:405– 407. 4. Xu L, Wang Y, Li Y, et al. Causes of blindness and visual impairment in urban and rural areas in Beijng. The Beijing Eye Study. Ophthalmology 2006;113:1134 –1141. 5. Curtin BJ, Teng CC. Scleral changes in pathological myopia. Trans Am Acad Ophthalmol Otolaryngol 1958;62:777–790. 6. Curtin BJ, Iwamoto T, Renaldo DP. Normal and staphylomatous sclera of high myopia: an electron microscopic study. Arch Ophthalmol 1979;97:912–915. 7. McBrien NA, Norton TT. Prevention of collagen crosslinking increases form deprivation myopia in tree shrew. Exp Eye Res 1994;59:475– 486. 8. Pruett RC. Complications associated with posterior staphyloma. Curr Opin Ophthalmol 1998;9:16 –22. 9. Curtin BJ. The posterior staphyloma of pathologic myopia. Trans Am Ophthal Soc 1977;75:67– 86. 10. Steidl SM, Pruett RC. Macular complications associated with posterior staphyloma. Am J Ophthalmol 1997;123:181– 187. 11. Avila MP, Weiter JJ, Jalkh AE, et al. Natural history of choroidal neovascularization in degenerative myopia. Ophthalmology 1984;91:1573–1581.
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Biosketch Huang Wei Hsiang, MD, graduated from Osaka University Medical School in 1999, and has been working at Tokyo Medical and Dental University since 2002. Dr Hsiang’s interest is on the development and progression of posterior staphyloma in pathologic myopia.
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SUPPLEMENTAL TABLE 1. The Relationship Between Grades of Myopic Degeneration and Grade of Posterior Staphyloma in Group 1 Variables
Grade 0 (21 Eyes)
Grade 1 (119 Eyes)
Grade 2 (45 Eyes)
Grade 3 (23 Eyes)
Grade 4 (one Eye)
Grades of myopic degeneration M0 M1 M2 M3 M4 M5
0 eyes (0%) 21 eyes (100%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%)
0 eyes (0%) 0 eyes (0%) 19 eyes (16%) 49 eyes (41.2%) 43 eyes (36.1%) Eight eyes (6.7%)
0 eyes (0%) 0 eyes (0%) Three eyes (6.7%) 14 eyes (31.1%) 17 eyes (37.8%) 11 eyes (24.4%)
0 eyes (0%) 0 eyes (0%) 0 eyes (0%) Seven eyes (30.4%) 12 eyes (52.2%) Four eyes (17.4%)
0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%) One eye (100%)
Depths of grade 1 staphyloma, ⱕ 2 mm; grade 2, ⬎ 2 mm but ⬍ 4 mm; grade 3, ⬎ 4 mm but ⬍ 6 mm; grade 4 staphyloma, ⬎ 6 mm. Grade M0 ⫽ normal-appearing posterior pole; grade M1 ⫽ choroidal pallor and tessellation; grade M2 ⫽ choroidal pallor and tessellation, with posterior staphyloma; grade M3 ⫽ choroidal pallor and tessellation, with posterior staphyloma and lacquer cracks; grade M4 ⫽ choroidal pallor and tessellation, with posterior staphyloma, lacquer cracks, and focal areas of deep choroidal atrophy; grade M5 ⫽ posterior pole with large geographic areas of deep choroidal atrophy (so-called bare sclera).
SUPPLEMENTAL TABLE 2. The Relationship between Grades of Myopic Degeneration and Grade of Posterior Staphyloma in Group 2 Variables
Grade 0 (21 Eyes)
Grade 1 (119 Eyes)
Grade 2 (45 Eyes)
Grade 3 (23 Eyes)
Grade 4 (One Eye)
Grades of myopic degeneration M0 M1 M2 M3 M4 M5
0 eyes (0%) 21 eyes (100%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%)
0 eyes (0%) 0 eyes (0%) 19 eyes (16%) 49 eyes (41.2%) 43 eyes (36.1%) Eight eyes (6.7%)
0 eyes (0%) 0 eyes (0%) Three eyes (6.7%) 14 eyes (31.1%) 17 eyes (37.8%) 11 eyes (24.4%)
0 eyes (0%) 0 eyes (0%) 0 eyes (0%) Seven eyes (30.4%) 12 eyes (52.2%) Four eyes (17.4%)
0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%) One eye (100%)
Depths of grade 1 staphyloma, ⱕ 2 mm; grade 2, ⬎ 2 mm but ⬍ 4 mm; grade 3, ⬎ 4 mm but ⬍ 6 mm; grade 4 staphyloma, ⬎ 6 mm. Grade M0 ⫽ normal-appearing posterior pole; grade M1 ⫽ choroidal pallor and tessellation; grade M2 ⫽ choroidal pallor and tessellation, with posterior staphyloma; grade M3 ⫽ choroidal pallor and tessellation, with posterior staphyloma and lacquer cracks; grade M4 ⫽ choroidal pallor and tessellation, with posterior staphyloma, lacquer cracks, and focal areas of deep choroidal atrophy; and grade M5 ⫽ posterior pole with large geographic areas of deep choroidal atrophy (so-called bare sclera).
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To determine the morphologic features (grade and type) of posterior staphylomas and to analyze the relationship between the morphologic features and the incidence of myopic macular lesions. ● DESIGN: Observational case series. ● METHODS: Two hundred and nine eyes of 108 consecutive patients with high myopia were studied. The grade of staphylomas was determined from B-scan ultrasonographic images across the optic disk. The type of staphyloma was determined by binocular funduscopy and was classified according to the criteria of Curtin. The participants were divided into two groups: younger than 50 years and 50 years and older. The long-term morphologic progression of staphylomas was analyzed in nine patients who were followed up for more than 20 years. ● RESULTS: Ninety percent of 209 eyes had a staphyloma. The prevalence of staphylomas and more advanced grades of staphylomas (> grade 2) were significantly higher in the older than in the younger patients. The higher grades of staphylomas were associated with more severe myopic retinal degeneration. Type II staphyloma was the most prominent overall; however, in older subjects, the incidence of type II was decreased significantly, and that of type IX was increased significantly. The eyes with type IX staphyloma tended to have more severe myopic retinal degeneration than eyes with type II staphylomas. The long-term follow-up study demonstrated a progression from type II to type IX with increasing age. ● CONCLUSIONS: These results suggest that the morphologic features of staphylomas worsens as the patient ages. The progression from type II to type IX probably increases the mechanical tension on the macular area of highly myopic eyes, which then leads to myopic fundus lesions. (Am J Ophthalmol 2008;146:102–110. © 2008 by Elsevier Inc. All rights reserved.)
Supplemental Material available at AJO.com. Accepted for publication Mar 4, 2008. From the Department of Ophthalmology and Visual Science, Tokyo Medical and Dental University, Bunkyo-ku, Tokyo, Japan. Inquiries to Kyoko Ohno-Matsui, Department of Ophthalmology and Visual Science, Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku, Tokyo 113, Japan; e-mail: [email protected]
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ATHOLOGIC MYOPIA IS ONE OF THE MOST FREQUENT
causes of secondary visual disturbances worldwide.1– 4 The prevalence of pathologic myopia is known to be different among races, and it is more common in the adult Asian population, at approximately 9%,2 than the 2% in the mainly White population in the United States of America.3 In the Beijing Eye Study of 4,409 Chinese individuals who were 40 years of age and older, pathologic myopia was the second most frequent cause of low vision and blindness.4 A posterior staphyloma is a protrusion of the posterior shell of the eye globe that frequently is found in highly myopic eyes and is considered to be a hallmark lesion. The scleral shell of highly myopic eyes has increased elasticity and a tendency to expand gradually and to thin. The collagen fibers in these eyes are pathologic5,6; the fibers are smaller in diameter, appear histologically immature, and may have fewer cross-linkages than those in emmetropic eyes.7 The development of a posterior staphyloma is accompanied by a stretching of the posterior fundus, resulting in various kinds of myopic lesions, for example, chorioretinal atrophy, choroidal neovascularization (CNV), macular retinoschisis, and macular holes. It is known that highly myopic eyes with a posterior staphyloma have a higher probability of having visual disturbances.8 Despite the importance of posterior staphylomas in highly myopic eyes, there have been few comprehensive studies on the morphologic features of posterior staphylomas.9 The most detailed study of posterior staphyloma was probably that carried out by Curtin 30 years ago.9 From our observations of more than 1,500 patients in our high myopia clinic over a period of 34 years, we hypothesize that a posterior staphyloma is present in a high percentage of patients with high myopia, and the morphologic features of the staphyloma change with increasing age. To test this hypothesis, we recruited 209 highly myopic eyes (108 consecutive patients), and the prevalence and the morphologic features (grades and types) of the staphylomas were determined for patients of different ages. Also, the longitudinal changes in the morphologic features of the posterior staphyloma were determined in nine patients who were followed up for more than 20 years in our high myopia clinic. Finally, we analyzed the relationship between the morphologic features of posterior staphyloma and the presence of myopic retinal degeneration.
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0002-9394/08/$34.00 doi:10.1016/j.ajo.2008.03.010
FIGURE 1. Illustration showing the classification of types of posterior staphyloma by Curtin.9
METHODS TWO HUNDRED AND NINE EYES OF 108 CONSECUTIVE PA-
tients with high myopia, refractive error of ⫺8.0 diopters (D) or more, or axial length of 26.5 mm or more were recruited prospectively from the High Myopia Clinic of the Tokyo Medical and Dental University between July 8, 2005 and December 16, 2005. Three eyes of three of these patients were not included because reliable ultrasonography could not be obtained because of dense cataracts. In addition, two eyes of two patients were not included because the eyes were not highly myopic, and two eyes of two patients also were not studied because of a history of posterior segment surgery (retinal detachment surgery and vitrectomy). The evaluations included refraction, axial length measurements, best-corrected visual acuity, detailed fundus drawings using indirect stereoscopic ophthalmoscopy, fluorescein angiography (FA), color fundus photography, and B-scan and A-scan ultrasonography. Informed consent was obtained from all patients for the FA. The patients were divided into two groups according to their age: group 1 consisted of 88 eyes of 44 patients who were younger than 50 years, and group 2 included 121 eyes of 64 patients who were 50 years of age and older. The posterior staphylomas were classified into different types and different grades. The type of posterior staphyloma was determined by the location, size, and severity (Figure 1)9 and was classified by binocular stereoscopic ophthalmoscopy. The staphylomas were classified into 10 types: types I through V were primary staphylomas, and types IV through X were compound staphylomas (Figure 1).9 The grade of the posterior staphyloma was determined from the B-scan and A-scan ultrasonographic images based on the criteria of Steidl and Pruett.10 The staphylomas were graded from zero to four based on the depth of the staphyloma measured on A-scan and B-scan ultrasonographic images obtained by Ultrascan (Alcon Surgical, Inc, Fort Worth, Texas, USA). The depth of the staphyloma was measured on a horizontal B-scan image across the VOL. 146, NO. 1
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FIGURE 2. Ultrasonography image showing the measurement of the grade of posterior staphyloma. The distance between the optic nerve plane and the deepest portion of the staphyloma is measured in a horizontal section of a B-mode ultrasonogram.
optic nerve head as the distance from the inner surface of the optic nerve head to the deepest part of the staphyloma (Figure 2). To ensure that the B-scan passed through the deepest part of the staphyloma, B scans were performed until five well-defined images were obtain from each eye. Because the variance of the depth of the staphyloma of each eye was small, we selected the average distance from the optic nerve head to the deepest part of the staphyloma for the grading. An elongated eye with a smooth scleral contour was graded as zero. A grade 1 staphyloma had a depth of 2 mm or less, a grade 2 staphyloma had a depth of more than 2 mm but less than 4 mm, a grade 3 staphyloma had a depth of more than 4 mm but less than 6 mm, and a grade 4 staphyloma had a depth of more than 6 mm. The same examiners (B.W.H., K.O.-M., T.Y.) determined the type and grade of the staphyloma in all of the IN
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eyes in a masked manner. Assessments of the intergrader and intragrader showed that the reliability was very good. Among the 108 patients, there were 15 eyes of nine patients who were followed up for more than 20 years. In each patient, the type of staphyloma was determined by stereoscopic fundus observations by three or more ophthalmologists independently at the initial visit, and each patient was examined at least once yearly thereafter. For these nine patients, the medical records and fundus photographs were analyzed retrospectively, and the long-term changes of the staphyloma were determined. The relationship between the morphologic features of staphyloma and myopic retinal degeneration also was analyzed in all patients. The degree of myopic chorioretinal changes was categorized in each patient according to the criteria of Avila and associates.11 The myopic fundus changes (M) were graded on a scale of increasing severity from zero to five: grade M0, normal-appearing posterior pole; grade M1, choroidal pallor and tessellation; grade M2, choroidal pallor and tessellation, with posterior staphyloma; grade M3, choroidal pallor and tessellation, with posterior staphyloma and lacquer cracks; grade M4, choroidal pallor and tessellation, with posterior staphyloma, lacquer cracks, and focal areas of deep choroidal atrophy; and grade M5, posterior pole with large geographic areas of deep choroidal atrophy (so-called bare sclera). The presence of CNV was determined by indirect ophthalmoscopy and fluorescein fundus angiography. The optical coherence tomography (OCT) examinations were performed through a dilated pupil using a commercially available OCT ophthalmoscope (C7; NIDEK, Aichi, Japan). Ten or more horizontal and vertical OCT scans (approximately 7 mm in length) were recorded in the macular area of each patient. The OCT images were analyzed carefully for the presence of macular holes, macular retinoschisis, and retinal detachments. The significance of differences in the data was determined by Fisher exact probability tests and Mann–Whitney U tests. A P value of less than .05 was considered statistically significant. For patients who had two eyes involved, only the data from the right eye was used for the statistical analyses.
TABLE 1. Patients and Study Eye Characteristics in Different Age Groups
Characteristics
Age (yrs), mean (SD) 39.0 (9.2) Reractive error (D), ⫺13.0 (4.3) mean (SD) Axial length (mm), 28.9 (1.9) mean (SD) Grades of myopic degeneration 0 M0 17 M1 13 M2 34 M3 24 M4 0 M5 Choroidal 15 neovascularization
P value
66.0 (8.5) ⫺13.0 (6.0)
⬍.0001* n.s.
29.2 (1.8)
n.s.
0 4 9 36 48 24 28
● GRADE OF POSTERIOR STAPHYLOMAS: The distribution of the grades of posterior staphylomas is shown in Table 2. Overall, 90% of all patients had a posterior staphyloma, and a grade 1 staphyloma was the most prevalent staphyloma observed, followed by grade 2. In group 1, 71 eyes (80.7%) had evidence of a staphyloma, and the grade 1 staphyloma was found in 64 eyes (72.7%) of the eyes. In group 1, staphylomas classified as grade 3 of higher were not detected. In group 2, 117 eyes (96.7%) of the eyes had a staphyloma, and the prevalence of a posterior staphyloma was significantly higher in group 2 than in group 1 (P ⫽ .0002). The prevalence of grade 1 was significantly lower in group 2 (45.5%) than in group 1 (72.7%). However, the prevalence of grade 2 was higher in group 2 (at 31.4%) than in group 1. In addition, the deeper staphylomas (grades 3 and 4) were found only in group 2. The differences in the prevalence of grade 1 and grade 2 staphylomas between groups 1 and 2 were statistically significant (P ⫽ .0001 and P ⬍ .0001, respectively). The axial lengths of eyes classified with grade 0 staphylomas were significantly shorter than all eyes with a staphyloma in both groups. However, the differences in the axial length between eyes with grades 1 and 2 and between grades 1 and 3 were not significant.
THE CHARACTERISTICS OF THE 108 PATIENTS (209 EYES) ARE
summarized in Table 1. There were 34 men and 74 women with a mean age of 55.0 ⫾ 14.9 years and a range of 23 to 78 years. The mean refractive error (spherical equivalent) was ⫺13.0 ⫾ 5.5 D, with a range ⫺8.5 to ⫺26.0 D, and the mean axial length was 29.3 ⫾ 1.9 mm, with a range of 26.5 to 33.0 mm. The differences in the refractive error and axial length between two groups were not significant. AMERICAN JOURNAL
Group 2 (ⱖ 50 yrs)
D ⫽ diopters; n.s. ⫽ not significant; SD ⫽ standard deviation. *Mann–Whitney U test.
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● TYPES OF POSTERIOR STAPHYLOMA:
The distribution of the different types of posterior staphyloma is summarized in Table 3. Types IV, VI, VII, VIII, and X were not observed in any of the eyes. The type II staphyloma was the most prevalent in both groups: 67.6% in group 1 and 43.6% in group 2. However, the prevalence of type II
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TABLE 2. Grades of Posterior Staphyloma and Axial Length in Different Age Groups Total
Group 1 (⬍50 yrs)
Group 2 (ⱖ 50 yrs)
Grades
No. (%)
Axial Length (mm)
No. (%)
Axial Length (mm)
No. (%)
Axial Length (mm)
0 1 2 3 4
21 eyes (10.0) 119 eyes (56.9) 45 eyes (21.5) 23 eyes (11.0) One eye (0.5)
27.0 ⫾ 1.13 29.0 ⫾ 1.68 29.9 ⫾ 1.57 29.7 ⫾ 1.28 31.3
17 eyes (19.3) 64 eyes (72.7) Seven eyes (8.0) 0 0
27.2 ⫾ 1.19 29.0 ⫾ 1.73 30.3 ⫾ 0.99 — —
4 eyes (3.3) 55 eyes (45.5) 38 eyes (31.4) 23 eyes (26.1) One eye (0.8)
26.5 ⫾ 0.39 29.1 ⫾ 1.61 29.8 ⫾ 1.66 29.7 ⫾ 1.28 31.3
The prevalence of grade 2 staphyloma was significantly higher in patients older than 50 years than in those younger than 50 years.
TABLE 3. Types of Posterior Staphyloma and Axial Length in Different Age Groups Total
Group 1 (⬍ 50 yrs)
Group 2 (ⱖ 50 yrs)
Types
No. (%)
Axial Length (mm)
No. (%)
Axial Length (mm)
No. (%)
Axial Length (mm)
I II III IV V VI VII VIII IX X
44 eyes (23.4) 99 eyes (52.7) 8 eyes (4.3) 0 5 eyes (2.7) 0 0 0 32 eyes (17.0) 0
29.1 ⫾ 1.92 29.2 ⫾ 1.64 27.5 ⫾ 1.20 — 29.1 ⫾ 0.18 — — — 30.1 ⫾ 1.63 —
13 eyes (18.3) 48 eyes (67.6) 6 eyes (8.5) 0 3 eyes (4.2) 0 0 0 1 eye (1.4) 0
28.8 ⫾ 1.54 29.4 ⫾ 1.21 26.9 ⫾ 0.71 — 28.9 ⫾ 0.23 — — — 30.5 —
31 eyes (26.5) 51 eyes (43.6) 2 eyes (1.7) 0 2 eyes (1.7) 0 0 0 31 eyes (26.5) 0
29.3 ⫾ 2.08 29.0 ⫾ 1.54 29.6 ⫾ 0.44 — 29.3 ⫾ 0.15 — — — 30.3 ⫾ 1.62 —
staphyloma was significantly higher in group 1 than in group 2 (P ⫽ .009). The major difference between the two groups was an increase in the prevalence of type IX staphyloma in group 2. A type IX staphyloma was seen in only one eye (1.4%) of group 1, but in 31 eyes (26.5%) in group 2 (P ⬍ .0001). In type IX staphylomas, a vertical septum with a width of one to two disk diameters was observed to pass from the upper to the lower border of the staphyloma (Figure 1).9 In all patients in group 1, the axial length of eyes with type III staphylomas was significantly shorter than that of eyes with each of the other types of staphylomas. In addition, the differences in the axial length between eyes with types I, II, and V staphylomas in all patients as well as between groups 1 and 2 were not significant. In group 2, the axial length of eyes with type IX staphylomas was significantly longer than eyes with types I and II staphylomas (P ⫽ .03 and .007, respectively). ● MYOPIC FUNDUS LESIONS AND GRADES OR TYPES OF POSTERIOR STAPHYLOMA: Eyes classified as M1, M2,
and M3, were categorized as having mild myopic retinal degeneration, and eyes classified as M4 and M5 were grouped as having severe myopic degeneration (Table 1). In group 1, 24 (27.3%) of 88 eyes had severe myopic degeneration, and in group 2, 71 (58.7%) of 121 eyes had severe myopic degeneration (Table 1). This difference was VOL. 146, NO. 1
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statistically significant (P ⬍ .0001). CNV was detected in 15 eyes (17.0%) in group 1 and in 28 eyes (23.1%) in group 2. This difference was not statistically significant. The relationships between myopic fundus lesions and the grade of the posterior staphyloma are summarized in Figure 3 and Table 4. Overall, our data showed that the higher the grade of the posterior staphyloma, the more severe the retinal degeneration tended to be (Figure 3). None of the eyes with grade 0 staphyloma had severe degeneration (M4 and M5), but 42.8% with grade 1 staphyloma had severe degeneration, 62.2% with grade 2 staphyloma had severe degeneration, 69.6% with grade 3 staphyloma had severe degeneration, and 100% with grade 4 staphyloma had severe degeneration. Although there was an increase in the prevalence of severe degeneration with an increase in the depth of the staphyloma, the differences among grades 1, 2, and 3 did not reach statistical significance. Because the patient age also may affect the grade of the myopic degeneration, we examined the grades of myopic degeneration in group 1 and in group 2 separately. The results demonstrated that even in older patients (group 2), the higher grades of posterior staphyloma were related to the development of more severe retinopathy (see Supplemental Tables 1 and 2 at AJO.com). A CNV was detected in 43 eyes (20.6%), lacquer cracks in 44 eyes (21.1%), macular retinoschisis in 24 eyes (11.5%), and macular holes in six eyes (2.9%) among all of IN
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excluded types III and V from the statistical analyses because the macular area was not included within the staphylomatous area in these two types. The prevalence of CNVs, active CNVs, and macular retinoschisis were not significantly different among eyes classified as types I, II, and IX staphylomas. However, eyes with lacquer cracks were detected significantly more frequently in eyes with type IX compared with type I staphyloma (P ⫽ .03) as well as with type II staphylomas (P ⬍ .001). ● LONG-TERM CHANGES IN POSTERIOR STAPHYLOMAS:
Fifteen eyes of nine patients were followed up for more than 20 years in our high myopia clinic. The clinical data of these nine patients are summarized in Table 6. The type of posterior staphyloma was determined by binocular indirect ophthalmoscopy at each follow-up examination by three or more ophthalmologists. At the initial examination, a posterior staphyloma was detected in 10 of 15 eyes, and all were classified as type II. Three eyes of three patients showed a change from type II to type IX staphyloma at 17 years (Case 1 in Table 6), 15 years (Case 2 in Table 6), and 18 years (Case 3 in Table 6) after the initial examination (Figure 5). In these patients, a ridge-like protrusion developed temporal to the optic disk at ages between their late 40s through the early 50s and transformed the staphyloma to type IX. In these three eyes that showed the progression of the type of staphyloma, a progression of myopic degeneration also was observed (Table 6). In contrast, in the other 12 eyes that did not show a change of the type of the posterior staphyloma, only two eyes showed a progression of myopic retinal degeneration.
FIGURE 3. Bar graph demonstrating the frequency of different grades of myopic degeneration as a function of the different grades of posterior staphyloma. The data showed that the higher the grade of the posterior staphyloma, the more severe the myopic retinal degeneration tended to be.
the 209 eyes. None of these types of lesion, that is, CNV, lacquer cracks, macular retinoschisis, and macular holes, was detected in eyes with grade 0 staphyloma. A CNV was detected in approximately 20% of the patients with grade 1 to 3 staphyloma, although the prevalence of CNVs was not significantly different among grades 1 to 3. Even when we examined the prevalence of the active phase of CNV only, there was no significant difference in the prevalence of active CNV among grades 1 to 3. The prevalence of lacquer cracks tended to increase as the grade of the staphyloma increased from grade 1 to 3, although the differences were not significant. Statistical analysis showed that macular retinoschisis was present significantly more frequently in eyes with grade 3 staphyloma than in eyes with grade 1 (P ⫽ .03). Macular holes were detected in only one to three eyes among grades 1 to 3. The distribution of the myopic fundus lesions and the types of posterior staphyloma is shown in Figure 4 and Table 5. Fifty percent of the eyes with type I staphyloma had severe retinal degeneration, 46.5% of eyes with type II staphyloma had severe degeneration, 50% of eyes with type III staphyloma had severe degeneration, none of the eyes with type V staphyloma had severe degeneration, and 71.9% of the eyes with type IX staphyloma had severe degeneration. Statistical analysis demonstrated that the eyes with type IX staphyloma had significantly more severe myopic retinal degeneration than those with type II staphyloma (P ⫽ .01). However, the difference in the prevalence of severe myopic retinal degeneration in eyes with type I and type IX staphylomas was not significant. The prevalence of severe myopic retinal degeneration in eyes with type I and type II staphyloma was significantly lower than in eyes with type IX staphyloma (P ⫽ .02). We 106
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in 90% of the patients with high myopia, and the prevalence of staphylomas was significantly higher in older patients (96.7% in those 50 years of age and older) than in younger patients (80.7% in patients younger than 50 years). Stiedl and Pruett10 reported that 88 (75.9%) of 116 eyes had a posterior staphyloma; however, they analyzed eyes with myopia ranging from ⫺3 to ⫺38 D with a mean of ⫺14 D. Thus, it is difficult to compare the prevalence of posterior staphylomas between the two studies, because the definition of myopia was different. The prevalence of grade 2 staphyloma was significantly higher in patients older than 50 years than in those younger than 50 years. This indicates that not only the incidence of posterior staphyloma but also the depth of the staphyloma increased as the patient ages. Interestingly, the axial length was not significantly different between eyes with grade 1 to 3 staphyloma. However, if we follow the changes in the grade of staphyloma in the same patient, it may be expected that the axial length would OF
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TABLE 4. The Relationship between Myopic Fundus Lesions and Grade of Posterior Staphyloma Variables
Choroidal neovascularization Choroidal neovascularization (active phase) Lacquer cracks Macular retinoschisis Macular holes Grades of myopic degeneration M0 M1 M2 M3 M4 M5
Grade 0 (21 Eyes)
Grade 1 (119 Eyes)
Grade 2 (45 Eyes)
Grade 3 (23 Eyes)
Grade 4 (One Eye)
0 eyes (0%)
27 eyes (22.7%)
11 eyes (24.4%)
Five eyes (21.7%)
0 eye (0%)
0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%)
Six eyes (5.0%) 23 eyes (19.3%) 11 eyes (9.2%) One eye (0.8%)
Two eyes (4.4%) 13 eyes (28.9%) Seven eyes (15.6%) Three eyes (6.7%)
One eye (4.3%) Eight eyes (34.8%) Six eyes (26.1%) Two eyes (8.7%)
0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%)
0 eyes (0%) 0 eyes (0%) 19 eyes (16.0%) 49 eyes (41.2%) 43 eyes (36.1%) Eight eyes (6.7%)
0 eyes (0%) 0 eyes (0%) Three eyes (6.7%) 14 eyes (31.1%) 17 eyes (37.8%) 11 eyes (24.4%)
0 eyes (0%) 0 eyes (0%) 0 eyes (0%) Seven eyes (30.4%) 12 eyes (52.2%) Four eyes (17.4%)
0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%) One eye (100%)
0 eyes (0%) 21 eyes (100%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%)
The data showed that the higher the grade of the posterior staphyloma, the more severe the retinal degeneration tended to be.
FIGURE 4. Bar graph demonstrating the frequency of different grades of myopic degeneration as a function of the different types of posterior staphyloma. The data showed that the frequency of the grade of myopic degeneration varied among the different types of staphylomas; however, eyes with type IX staphyloma had more severe myopic retinal degeneration than those with type II staphyloma.
increase with an increase in the grade of staphyloma. However, this was not found, probably because there was a wide range of axial lengths in eyes with a staphyloma at the initial examination. Curtin also reported an unusually wide range of refractive errors and axial lengths for eyes with the same type of staphyloma.9 The type II staphylomas were the most prominent type in groups 1 and 2. In contrast, Curtin reported that type I was the most prominent and was observed in 55% of the eyes with a posterior staphyloma, and the type II was observed in only 8.4% of the eyes examined (calculated from his Table II).9 Oie and associates examined the types VOL. 146, NO. 1
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of staphyloma in 28 Japanese with highly myopic eyes with a macular hole retinal detachment (MHRD) and in 47 highly myopic eyes without an MHRD.12 They reported that in the eyes with an MHRD, 19% had type I staphyloma and 63% had type II staphyloma, whereas in the group without an MHRD, 43% had type I staphyloma and 25% had type II staphyloma. Although the number of their patients was much smaller, their results also indicated that the prevalence of type II staphyloma was higher in Japanese patients than that reported by Curtin (who mainly studied White persons).9 In group 2, the prevalence of type II staphylomas was lower than in group 1, and instead, type IX staphyloma increased. In type IX staphyloma, a ridge-like protrusion was present temporal to the optic disk. And more importantly, in the patients who were followed up for more than 20 years, the ridge-like protrusion developed in the three patients who demonstrated the progression from type II to type IX staphyloma. These findings suggest that type IX staphylomas develop secondarily by the development of a ridge-like protrusion temporal to the optic disk in eyes originally with type II staphyloma as the patient ages. Therefore, our results indicated that the posterior staphyloma not only deepens, but its morphologic features also change as the patients grow older. This is important because these morphologic changes of the posterior staphyloma enhance the development of severe myopic retinal degeneration. The sclera is a typical connective tissue and consists of interwoven collagen fibrils in close association with proteoglycans. The number, arrangement, and types of collagen fibrils are considered to determine the mechanical strength of a sclera. The reason why the morphologic features of posterior staphyloma worsen with increasing age has not been clarified fully, and some authors have reported alterations in the composition of the sclera extracellular matrix in humans13,14 as well as animals.15 IN
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TABLE 5. The Relationship between Myopic Fundus Lesions and Type of Posterior Staphyloma Variables
Type I (44 Eyes)
Type II (99 Eyes)
Type III (8 Eyes)
Choroidal neovascularization Choroidal neovascularization (active phase) Lacquer cracks Macular retinoschisis Macular holes Grades of myopic degeneration M0 M1 M2 M3 M4 M5
Seven eyes (15.9%)
23 eyes (23.2%)
Two eyes (4.5%) 11 eyes (25%) Nine eyes (20.5%) Two eyes (4.5%) 0 eyes (0%) 0 eyes (0%) Two eyes (4.5%) 20 eyes (45.5%) 10 eyes (22.7%) 12 eyes (27.3%)
Type V (5 Eyes)
Type IX (32 Eyes)
Three eyes (37.5%)
0 eyes (0%)
10 eyes (31.3%)
Five eyes (5.1%) 17 eyes (17.2%) Nine eyes (9.1%) Two eyes (2.0%)
0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%)
0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%)
Two eyes (6.3%) 16 eyes (50%) Six eyes (18.8%) Two eyes (6.3%)
0 eyes (0%) 0 eyes (0%) 15 eyes (15.2%) 38 eyes (38.4%) 38 eyes (38.4%) Eight eyes (8.1%)
0 eyes (0%) 0 eyes (0%) Three eyes (37.5%) One eyes (12.5%) Four eyes (50%) 0 eyes (0%)
0 eyes (0%) 0 eyes (0%) One eyes (20%) Four eyes (80%) 0 eyes (0%) 0 eyes (0%)
0 eyes (0%) 0 eyes (0%) Two eyes (6.3%) Seven eyes (21.9%) 19 eyes (59.4%) Four eyes (12.5%)
TABLE 6. Characteristics of Patients with Long-Term Follow-up and the Long-Term Change of the Type of Posterior Staphyloma At Initial Examination Patient Age Refractive Axial Length Type of Myopic Age No. Sex Eye (yrs) Error (D) (mm) Staphyloma Degeneration* (yrs)
1 2
F F
3 4 5
F F F
6
F
7
M
8
F
9
M
R R L R L R L R L R L R L R L
42 48 47 48 44 29 50 35 35
⫺22.0 ⫺20.0 ⫺13.0 ⫺9.0 ⫺13.0 ⫺19.0 ⫺15.0 ⫺14.0 ⫺16.0 ⫺14.0 ⫺12.0 ⫺11.0 ⫺12.0 ⫺23.0 ⫺11.0
31.9 31.8 29.0 27.8 29.0 28.4 27.9 28.8 29.3 27.2 27.0 29.7 29.9 30.9 29.1
II II II II II II II II II 0 0 0 0 II 0
M4 M3 M3 M2 M3 M3 M3 M3 M3 M1 M1 M1 M1 M2 M1
68 70 74 70 66 49 70 58 58
Refractive Error (D)
⫺8.0 (IOL) ⫺6.0 (IOL) ⫺5.0 (IOL) ⫺4.25 (IOL) ⫺5.0 (IOL) ⫺19.0 ⫺15.0 ⫺18.0 ⫺18.0 ⫺15.0 ⫺15.0 ⫺11.0 ⫺12.5 ⫺23.0 ⫺11.5
At Final Examination Change of Axial Length Type of Myopic Type of Follow-up (mm) Staphyloma Degeneration* Staphyloma (yrs)
33.3 32.4 29.8 28.6 29.8 29.7 29.3 29.9 29.5 28.0 27.6 30.6 30.8 33.8 29.4
IX IX II IX II II II II II 0 0 0 0 II 0
M5 M4 M3 M3 M3 M4 M3 M3 M3 M1 M1 M1 M1 M3 M1
Y Y N Y N N N N N N N N N N N
26 22 27 22 22 29 20 23 23
D ⫽ diopter; F ⫽ female; IOL ⫽ intraocular lens; L ⫽ left; M ⫽ male; N ⫽ no; R ⫽ right; Y ⫽ yes. *See Methods for classification.
opment of macular retinoschisis. Although the mechanism of macular retinoschisis development has not been clarified fully, some causative factors such as the presence of vascular microfolds,18 paravascular inner lamellar hole,19 and subsequent tractional detachment of inner limiting membrane20 have been suggested. An increased mechanical tension caused by an increased depth of posterior staphyloma may facilitate these proposed causative factors. Stiedl and Pruett10 reported that the eyes with the shallowest staphyloma (grade 1) had the highest frequency of CNV. They suggested that it is possible that the grade 1 eyes may be healthier and more metabolically active with well-perfused chorioretinal tissue and good capacity to respond to injury by neovascular ingrowth. In contrast, the
Our results showed that the higher grades of staphyloma were associated with more severe myopic retinal degeneration, which was similar to the results previously reported by Stiedl and Pruett.10 Curtin and Karlin also reported a strong correlation between axial length and myopic chorioretinal atrophy, although the correlation between the myopic chorioretinopathy and posterior staphyloma was not reported.16 Among the independent myopic macular lesions, the prevalence of macular retinoschisis was significantly higher in eyes with grade 3 staphylomas compared with those with grade 1 staphylomas. We have reported that macular retinoschisis was detected only in highly myopic eyes with a posterior staphyloma,17 which supports the idea on the importance of staphylomas in the devel108
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FIGURE 5. Fundus photographs showing the progression from type II to type IX staphyloma (right fundus of Case 1 in Table 6). (Left) Right fundus of a 42-year-old woman. Refractive error was ⴚ22.0 diopters and the axial length was 31.9 mm. Type II staphyloma is visible (arrowheads), and the posterior fundus shows fibrovascular tissue (arrow) and focal chorioretinal atrophy. (Right) Twenty-six years later, the axial length of the same eye was 33.3 mm. A ridge-like protrusion can be seen temporal to the optic disk (arrows), and the type of staphyloma has progressed to type IX. Focal chorioretinal atrophy has spread widely and the posterior fundus shows a bare sclera appearance. The optic disk also is stretched vertically.
prevalence of CNV (total CNV and active CNV) was not different among different grades of staphylomas in our study. The reason for this discrepancy is not clear; however, one reason may be a difference in the classification of high myopia (⬎ ⫺3.0 D vs ⬎ ⫺8.0 D). Thus, it is possible that some of the CNVs in their study may have been nonmyopic in origin (e.g., idiopathic CNV). Our results showed that eyes with type IX staphylomas had severe myopic retinal degeneration more frequently than eyes with type II staphylomas (Table 5). In addition, the axial length of eyes with type IX staphyloma was significantly longer than those with type II staphyloma. We suggest that there is an increase in the mechanical tension on the posterior pole as well as on the optic disk by the ridge-like protrusion in eyes of type IX staphyloma and that this probably facilitates the development and progression of myopic retinal degeneration. The prevalence of lacquer cracks was significantly higher in eyes with type IX staphyloma than in those with type II staphyloma. Lacquer cracks are mechanical ruptures of the Bruch membrane caused by an axial elongation; therefore, an increased prevalence of lacquer cracks in eyes with type IX may reflect an increased mechanical expansion of the posterior fundus. One of the most interesting aspect of our study was that we were able to examine the morphologic features of the posterior staphyloma in 15 eyes of nine patients periodically for more than 20 years. The results showed the clear
progression from type II to type IX staphyloma in three patients. Our longitudinal study showed that all three of the eyes that showed a progression from type II to type IX staphyloma had a progression of myopic retinal degeneration, whereas only two of 12 eyes without the progression of the staphyloma showed a progression of the retinal degeneration. These findings indicate that the morphologic changes of the posterior staphyloma may be more important for the development or progression of myopic retinal degeneration than the axial length alone. In conclusion, we examined the grades and types of posterior staphyloma in a large number of Japanese patients with pathologic myopia. The results demonstrated that the type II staphyloma was the most prominent type in Japanese patients with high myopia. The grade of staphyloma and prevalence of type IX staphyloma was higher in older patients. These findings suggest that the posterior staphyloma not only deepens but also its morphologic features change as the patients age, even though the axial length does not change significantly. The longitudinal study revealed a clear progression from type II to type IX staphyloma in three of 15 patients. The progression to type IX staphyloma may be an important feature and may increase the mechanical tension on the macular area and optic disk, which may cause the progression to severe myopic retinal degeneration.
THIS STUDY WAS SUPPORTED IN PART BY RESEARCH GRANTS 16390495, 17591823, AND 19390441 FROM THE JAPAN SOCIETY FOR the Promotion of Science, Tokyo, Japan. The authors indicate no financial conflict of interest. Involved in design of study (H.W.H., K.O.-M.); conduct of study (H.W.H., K.O.-M., N.S., K.H., M.M., T.Y.); analysis and interpretation (H.W.H., N.S., K.H., M.M.); writing the article (H.W.H., K.O.-M.); critical revision of the article (K.O.-M., M.M., T.Y., T.T., M.M.); obtaining funding (K.O.-M., M.M.); literature search (H.W.H., K.O.-M., N.S., K.H.); and data collection (H.W.H., K.O.-M., N.S., K.H., M.M., T.Y.); review and approval of manuscript (K.O.M., T.T., M.M.) . Because the ultrasonography
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to measure the axial length and to evaluate the morphologic features of posterior staphyloma is performed routinely for highly myopic patients, the Institutional Review Board of the Tokyo Medical and Dental University determined that no approval to perform the examination is necessary. The procedures used conformed to the tenets of the Declaration of Helsinki. The authors thank Professor Duco Hamasaki, Bascom Palmer Eye Institute, Miami, Florida for his critical discussion in the early phase of this study and for the revision of the final manuscript.
12. Oie Y, Ikuno Y, Fujikado T, Tano Y. Relation of posterior staphyloma in highly myopic eyes with macular hole and retinal detachment. Jpn J Ophthalmol 2005;49:530 – 532. 13. Dunlevy JR, Summers Rada JA. Interaction of lumican with aggrecan in the aging human sclera. Invest Ophthalmol Vis Sci 2004;45:3849 –3856. 14. Rada JA, Achen VR, Penugonda S, Schmidt RW, Mount BA. Proteoglycan composition in the human sclera during growth and aging. Invest Ophthalmol Vis Sci 2000;41:1639 – 1648. 15. Albon J, Farrant S, Akhtar S, et al. Connective tissue structure of the tree shrew optic nerve and associated aging changes. Invest Ophthalmol Vis Sci 2007;48:2134 –2144. 16. Curtin BJ, Karlin DB. Axial length measurements and fundus changes of the myopic eye. Am J Ophthalmol 1971;71: 42–53. 17. Baba T, Ohno-Matsui K, Futagami S, et al. Prevalence and characteristics of foveal retinal detachment without macular hole in high myopia. Am J Ophthalmol 2003;135:338 –342. 18. Sayanagi K, Ikuno Y, Gomi F, Tano Y. Retinal vascular microfolds in highly myopic eyes. Am J Ophthalmol 2005; 139:658 – 663. 19. Shimada N, Ohno-Matsui K, Nishimuta A, et al. Detection of paravascular lamellar holes and other paravascular abnormalities by optical coherence tomography in eyes with high myopia. Ophthalmology 2008;115:708 –717. 20. Sayanagi K, Ikuno Y, Tano Y. Tractional internal limiting membrane detachment in highly myopic eyes. Am J Ophthalmol 2006;142:850 – 852.
REFERENCES 1. Ghafour IM, Allan D, Foulds WS. Common causes of blindness and visual handicap in the west of Scotland. Br J Ophthalmol 1983;67:209 –213. 2. Wong TY, Foster PJ, Hee J, et al. Prevalence and risk factors for refractive errors in adult Chinese in Singapore. Invest Ophthalmol Vis Sci 2000;41:2486 –2494. 3. Sperduto RD, Seigel D, Roberts J, et al. Prevalence of myopia in the United States. Arch Ophthalmol 1983;101:405– 407. 4. Xu L, Wang Y, Li Y, et al. Causes of blindness and visual impairment in urban and rural areas in Beijng. The Beijing Eye Study. Ophthalmology 2006;113:1134 –1141. 5. Curtin BJ, Teng CC. Scleral changes in pathological myopia. Trans Am Acad Ophthalmol Otolaryngol 1958;62:777–790. 6. Curtin BJ, Iwamoto T, Renaldo DP. Normal and staphylomatous sclera of high myopia: an electron microscopic study. Arch Ophthalmol 1979;97:912–915. 7. McBrien NA, Norton TT. Prevention of collagen crosslinking increases form deprivation myopia in tree shrew. Exp Eye Res 1994;59:475– 486. 8. Pruett RC. Complications associated with posterior staphyloma. Curr Opin Ophthalmol 1998;9:16 –22. 9. Curtin BJ. The posterior staphyloma of pathologic myopia. Trans Am Ophthal Soc 1977;75:67– 86. 10. Steidl SM, Pruett RC. Macular complications associated with posterior staphyloma. Am J Ophthalmol 1997;123:181– 187. 11. Avila MP, Weiter JJ, Jalkh AE, et al. Natural history of choroidal neovascularization in degenerative myopia. Ophthalmology 1984;91:1573–1581.
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Biosketch Huang Wei Hsiang, MD, graduated from Osaka University Medical School in 1999, and has been working at Tokyo Medical and Dental University since 2002. Dr Hsiang’s interest is on the development and progression of posterior staphyloma in pathologic myopia.
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SUPPLEMENTAL TABLE 1. The Relationship Between Grades of Myopic Degeneration and Grade of Posterior Staphyloma in Group 1 Variables
Grade 0 (21 Eyes)
Grade 1 (119 Eyes)
Grade 2 (45 Eyes)
Grade 3 (23 Eyes)
Grade 4 (one Eye)
Grades of myopic degeneration M0 M1 M2 M3 M4 M5
0 eyes (0%) 21 eyes (100%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%)
0 eyes (0%) 0 eyes (0%) 19 eyes (16%) 49 eyes (41.2%) 43 eyes (36.1%) Eight eyes (6.7%)
0 eyes (0%) 0 eyes (0%) Three eyes (6.7%) 14 eyes (31.1%) 17 eyes (37.8%) 11 eyes (24.4%)
0 eyes (0%) 0 eyes (0%) 0 eyes (0%) Seven eyes (30.4%) 12 eyes (52.2%) Four eyes (17.4%)
0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%) One eye (100%)
Depths of grade 1 staphyloma, ⱕ 2 mm; grade 2, ⬎ 2 mm but ⬍ 4 mm; grade 3, ⬎ 4 mm but ⬍ 6 mm; grade 4 staphyloma, ⬎ 6 mm. Grade M0 ⫽ normal-appearing posterior pole; grade M1 ⫽ choroidal pallor and tessellation; grade M2 ⫽ choroidal pallor and tessellation, with posterior staphyloma; grade M3 ⫽ choroidal pallor and tessellation, with posterior staphyloma and lacquer cracks; grade M4 ⫽ choroidal pallor and tessellation, with posterior staphyloma, lacquer cracks, and focal areas of deep choroidal atrophy; grade M5 ⫽ posterior pole with large geographic areas of deep choroidal atrophy (so-called bare sclera).
SUPPLEMENTAL TABLE 2. The Relationship between Grades of Myopic Degeneration and Grade of Posterior Staphyloma in Group 2 Variables
Grade 0 (21 Eyes)
Grade 1 (119 Eyes)
Grade 2 (45 Eyes)
Grade 3 (23 Eyes)
Grade 4 (One Eye)
Grades of myopic degeneration M0 M1 M2 M3 M4 M5
0 eyes (0%) 21 eyes (100%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%)
0 eyes (0%) 0 eyes (0%) 19 eyes (16%) 49 eyes (41.2%) 43 eyes (36.1%) Eight eyes (6.7%)
0 eyes (0%) 0 eyes (0%) Three eyes (6.7%) 14 eyes (31.1%) 17 eyes (37.8%) 11 eyes (24.4%)
0 eyes (0%) 0 eyes (0%) 0 eyes (0%) Seven eyes (30.4%) 12 eyes (52.2%) Four eyes (17.4%)
0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%) One eye (100%)
Depths of grade 1 staphyloma, ⱕ 2 mm; grade 2, ⬎ 2 mm but ⬍ 4 mm; grade 3, ⬎ 4 mm but ⬍ 6 mm; grade 4 staphyloma, ⬎ 6 mm. Grade M0 ⫽ normal-appearing posterior pole; grade M1 ⫽ choroidal pallor and tessellation; grade M2 ⫽ choroidal pallor and tessellation, with posterior staphyloma; grade M3 ⫽ choroidal pallor and tessellation, with posterior staphyloma and lacquer cracks; grade M4 ⫽ choroidal pallor and tessellation, with posterior staphyloma, lacquer cracks, and focal areas of deep choroidal atrophy; and grade M5 ⫽ posterior pole with large geographic areas of deep choroidal atrophy (so-called bare sclera).
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