Clinical Characteristics of Posterior Staphyloma in Eyes with Pathologic Myopia

●

(tt●

●

uogyciypw●

lghhswscTsssi●

lTchlb

A

M

VB

1

Clinical Characteristics of Posterior Staphyloma in Eyeswith Pathologic Myopia

HUANG WEI HSIANG, KYOKO OHNO-MATSUI, NORIAKI SHIMADA, KENGO HAYASHI,
MUKA MORIYAMA, TAKESHI YOSHIDA, TAKASHI TOKORO, AND MANABU MOCHIZUKI
PkitSCpl

smsacsme

nvarmp

hsmpomtoohcpwlpwmt

PURPOSE: To determine the morphologic featuresgrade and type) of posterior staphylomas and to analyzehe relationship between the morphologic features andhe incidence of myopic macular lesions. DESIGN: Observational case series. METHODS: Two hundred and nine eyes of 108 consec-tive patients with high myopia were studied. The gradef staphylomas was determined from B-scan ultrasono-raphic images across the optic disk. The type of staph-loma was determined by binocular funduscopy and waslassified according to the criteria of Curtin. The partic-pants were divided into two groups: younger than 50ears and 50 years and older. The long-term morphologicrogression of staphylomas was analyzed in nine patientsho were followed up for more than 20 years.

RESULTS: Ninety percent of 209 eyes had a staphy-oma. The prevalence of staphylomas and more advancedrades of staphylomas (> grade 2) were significantlyigher in the older than in the younger patients. Theigher grades of staphylomas were associated with moreevere myopic retinal degeneration. Type II staphylomaas the most prominent overall; however, in older

ubjects, the incidence of type II was decreased signifi-antly, and that of type IX was increased significantly.he eyes with type IX staphyloma tended to have more

evere myopic retinal degeneration than eyes with type IItaphylomas. The long-term follow-up study demon-trated a progression from type II to type IX withncreasing age. CONCLUSIONS: These results suggest that the morpho-ogic features of staphylomas worsens as the patient ages.he progression from type II to type IX probably in-

reases the mechanical tension on the macular area ofighly myopic eyes, which then leads to myopic fundusesions. (Am J Ophthalmol 2008;146:102–110. © 2008y Elsevier Inc. All rights reserved.)

Supplemental Material available at AJO.com.ccepted for publication Mar 4, 2008.From the Department of Ophthalmology and Visual Science, Tokyoedical and Dental University, Bunkyo-ku, Tokyo, Japan.Inquiries to Kyoko Ohno-Matsui, Department of Ophthalmology and

aisual Science, Tokyo Medical and Dental University, 1-5-45 Yushima,unkyo-ku, Tokyo 113, Japan; e-mail: [email protected]

© 2008 BY ELSEVIER INC. A02

ATHOLOGIC MYOPIA IS ONE OF THE MOST FREQUENT

causes of secondary visual disturbances world-wide.1–4 The prevalence of pathologic myopia is

nown to be different among races, and it is more commonn the adult Asian population, at approximately 9%,2 thanhe 2% in the mainly White population in the Unitedtates of America.3 In the Beijing Eye Study of 4,409hinese individuals who were 40 years of age and older,athologic myopia was the second most frequent cause ofow vision and blindness.4

A posterior staphyloma is a protrusion of the posteriorhell of the eye globe that frequently is found in highlyyopic eyes and is considered to be a hallmark lesion. The

cleral shell of highly myopic eyes has increased elasticitynd a tendency to expand gradually and to thin. Theollagen fibers in these eyes are pathologic5,6; the fibers aremaller in diameter, appear histologically immature, anday have fewer cross-linkages than those in emmetropic

yes.7

The development of a posterior staphyloma is accompa-ied by a stretching of the posterior fundus, resulting inarious kinds of myopic lesions, for example, chorioretinaltrophy, choroidal neovascularization (CNV), macularetinoschisis, and macular holes. It is known that highlyyopic eyes with a posterior staphyloma have a higher

robability of having visual disturbances.8

Despite the importance of posterior staphylomas inighly myopic eyes, there have been few comprehensivetudies on the morphologic features of posterior staphylo-as.9 The most detailed study of posterior staphyloma was

robably that carried out by Curtin 30 years ago.9 From ourbservations of more than 1,500 patients in our highyopia clinic over a period of 34 years, we hypothesize

hat a posterior staphyloma is present in a high percentagef patients with high myopia, and the morphologic featuresf the staphyloma change with increasing age. To test thisypothesis, we recruited 209 highly myopic eyes (108onsecutive patients), and the prevalence and the mor-hologic features (grades and types) of the staphylomasere determined for patients of different ages. Also, the

ongitudinal changes in the morphologic features of theosterior staphyloma were determined in nine patientsho were followed up for more than 20 years in our highyopia clinic. Finally, we analyzed the relationship be-

ween the morphologic features of posterior staphyloma
nd the presence of myopic retinal degeneration.
LL RIGHTS RESERVED. 0002-9394/08/$34.00doi:10.1016/j.ajo.2008.03.010

mailto:[email protected]

T

t(rT2ppabps

sdoBo

two

twaTVc

fowsgIl

ot(duBetfcdmha

F

Foom

V

METHODS

WO HUNDRED AND NINE EYES OF 108 CONSECUTIVE PA-

ients with high myopia, refractive error of �8.0 dioptersD) or more, or axial length of 26.5 mm or more wereecruited prospectively from the High Myopia Clinic of theokyo Medical and Dental University between July 8,005 and December 16, 2005. Three eyes of three of theseatients were not included because reliable ultrasonogra-hy could not be obtained because of dense cataracts. Inddition, two eyes of two patients were not includedecause the eyes were not highly myopic, and two eyes of twoatients also were not studied because of a history of posterioregment surgery (retinal detachment surgery and vitrectomy).

The evaluations included refraction, axial length mea-urements, best-corrected visual acuity, detailed fundusrawings using indirect stereoscopic ophthalmoscopy, flu-rescein angiography (FA), color fundus photography, and-scan and A-scan ultrasonography. Informed consent wasbtained from all patients for the FA.The patients were divided into two groups according to

heir age: group 1 consisted of 88 eyes of 44 patients whoere younger than 50 years, and group 2 included 121 eyesf 64 patients who were 50 years of age and older.The posterior staphylomas were classified into different

ypes and different grades. The type of posterior staphylomaas determined by the location, size, and severity (Figure 1)9

nd was classified by binocular stereoscopic ophthalmoscopy.he staphylomas were classified into 10 types: types I throughwere primary staphylomas, and types IV through X were

ompound staphylomas (Figure 1).9

The grade of the posterior staphyloma was determinedrom the B-scan and A-scan ultrasonographic images basedn the criteria of Steidl and Pruett.10 The staphylomasere graded from zero to four based on the depth of the

taphyloma measured on A-scan and B-scan ultrasono-raphic images obtained by Ultrascan (Alcon Surgical,nc, Fort Worth, Texas, USA). The depth of the staphy-

IGURE 1. Illustration showing the classification of types of p

oma was measured on a horizontal B-scan image across the m

POSTERIOR STAPHYLOMA INOL. 146, NO. 1

ptic nerve head as the distance from the inner surface ofhe optic nerve head to the deepest part of the staphylomaFigure 2). To ensure that the B-scan passed through theeepest part of the staphyloma, B scans were performedntil five well-defined images were obtain from each eye.ecause the variance of the depth of the staphyloma ofach eye was small, we selected the average distance fromhe optic nerve head to the deepest part of the staphylomaor the grading. An elongated eye with a smooth scleralontour was graded as zero. A grade 1 staphyloma had aepth of 2 mm or less, a grade 2 staphyloma had a depth ofore than 2 mm but less than 4 mm, a grade 3 staphylomaad a depth of more than 4 mm but less than 6 mm, andgrade 4 staphyloma had a depth of more than 6 mm.The same examiners (B.W.H., K.O.-M., T.Y.) deter-

rior staphyloma by Curtin.9

IGURE 2. Ultrasonography image showing the measurementf the grade of posterior staphyloma. The distance between theptic nerve plane and the deepest portion of the staphyloma iseasured in a horizontal section of a B-mode ultrasonogram.

oste

ined the type and grade of the staphyloma in all of the

PATHOLOGIC MYOPIA 103

ea

pesmpttc

santcfpclprladea

waTiofa

mnsis

T

sw7wt2a

●

tTspgaoh

sw.ipt(dss

lsag

●

oiot

1

yes in a masked manner. Assessments of the intergradernd intragrader showed that the reliability was very good.

Among the 108 patients, there were 15 eyes of nineatients who were followed up for more than 20 years. Inach patient, the type of staphyloma was determined bytereoscopic fundus observations by three or more ophthal-ologists independently at the initial visit, and each

atient was examined at least once yearly thereafter. Forhese nine patients, the medical records and fundus pho-ographs were analyzed retrospectively, and the long-termhanges of the staphyloma were determined.

The relationship between the morphologic features oftaphyloma and myopic retinal degeneration also wasnalyzed in all patients. The degree of myopic chorioreti-al changes was categorized in each patient according tohe criteria of Avila and associates.11 The myopic fundushanges (M) were graded on a scale of increasing severityrom zero to five: grade M0, normal-appearing posteriorole; grade M1, choroidal pallor and tessellation; grade M2,horoidal pallor and tessellation, with posterior staphy-oma; grade M3, choroidal pallor and tessellation, withosterior staphyloma and lacquer cracks; grade M4, cho-oidal pallor and tessellation, with posterior staphyloma,acquer cracks, and focal areas of deep choroidal atrophy;nd grade M5, posterior pole with large geographic areas ofeep choroidal atrophy (so-called bare sclera). The pres-nce of CNV was determined by indirect ophthalmoscopynd fluorescein fundus angiography.

The optical coherence tomography (OCT) examinationsere performed through a dilated pupil using a commerciallyvailable OCT ophthalmoscope (C7; NIDEK, Aichi, Japan).en or more horizontal and vertical OCT scans (approx-

mately 7 mm in length) were recorded in the macular areaf each patient. The OCT images were analyzed carefullyor the presence of macular holes, macular retinoschisis,nd retinal detachments.

The significance of differences in the data was deter-ined by Fisher exact probability tests and Mann–Whit-ey U tests. A P value of less than .05 was consideredtatistically significant. For patients who had two eyesnvolved, only the data from the right eye was used for thetatistical analyses.

RESULTS

HE CHARACTERISTICS OF THE 108 PATIENTS (209 EYES) ARE

ummarized in Table 1. There were 34 men and 74 womenith a mean age of 55.0 � 14.9 years and a range of 23 to8 years. The mean refractive error (spherical equivalent)as �13.0 � 5.5 D, with a range �8.5 to �26.0 D, and

he mean axial length was 29.3 � 1.9 mm, with a range of6.5 to 33.0 mm. The differences in the refractive error
nd axial length between two groups were not significant. 4
AMERICAN JOURNAL OF04

GRADE OF POSTERIOR STAPHYLOMAS: The distribu-ion of the grades of posterior staphylomas is shown inable 2. Overall, 90% of all patients had a posterior

taphyloma, and a grade 1 staphyloma was the mostrevalent staphyloma observed, followed by grade 2. Inroup 1, 71 eyes (80.7%) had evidence of a staphyloma,nd the grade 1 staphyloma was found in 64 eyes (72.7%)f the eyes. In group 1, staphylomas classified as grade 3 ofigher were not detected.In group 2, 117 eyes (96.7%) of the eyes had a

taphyloma, and the prevalence of a posterior staphylomaas significantly higher in group 2 than in group 1 (P �

0002). The prevalence of grade 1 was significantly lowern group 2 (45.5%) than in group 1 (72.7%). However, therevalence of grade 2 was higher in group 2 (at 31.4%)han in group 1. In addition, the deeper staphylomasgrades 3 and 4) were found only in group 2. Theifferences in the prevalence of grade 1 and grade 2taphylomas between groups 1 and 2 were statisticallyignificant (P � .0001 and P � .0001, respectively).

The axial lengths of eyes classified with grade 0 staphy-omas were significantly shorter than all eyes with ataphyloma in both groups. However, the differences in thexial length between eyes with grades 1 and 2 and betweenrades 1 and 3 were not significant.

TYPES OF POSTERIOR STAPHYLOMA: The distributionf the different types of posterior staphyloma is summarizedn Table 3. Types IV, VI, VII, VIII, and X were notbserved in any of the eyes. The type II staphyloma washe most prevalent in both groups: 67.6% in group 1 and

TABLE 1. Patients and Study Eye Characteristics inDifferent Age Groups

Characteristics

Group 1

(� 50 yrs)

Group 2

(� 50 yrs)

P

value

Age (yrs), mean (SD) 39.0 (9.2) 66.0 (8.5) �.0001*

Reractive error (D),

mean (SD)

�13.0 (4.3) �13.0 (6.0) n.s.

Axial length (mm),

mean (SD)

28.9 (1.9) 29.2 (1.8) n.s.

Grades of myopic

degeneration

M0 0 0

M1 17 4

M2 13 9

M3 34 36

M4 24 48

M5 0 24

Choroidal

neovascularization

15 28

D � diopters; n.s. � not significant; SD � standard deviation.

*Mann–Whitney U test.

3.6% in group 2. However, the prevalence of type II

OPHTHALMOLOGY JULY 2008

sggsogsos

teawatsl

●

P

adgIds

s1g

tFhsNdss3gtetsat2pw(

i

patie

V

taphyloma was significantly higher in group 1 than inroup 2 (P � .009). The major difference between the tworoups was an increase in the prevalence of type IXtaphyloma in group 2. A type IX staphyloma was seen innly one eye (1.4%) of group 1, but in 31 eyes (26.5%) inroup 2 (P � .0001). In type IX staphylomas, a verticaleptum with a width of one to two disk diameters wasbserved to pass from the upper to the lower border of thetaphyloma (Figure 1).9

In all patients in group 1, the axial length of eyes withype III staphylomas was significantly shorter than that ofyes with each of the other types of staphylomas. Inddition, the differences in the axial length between eyesith types I, II, and V staphylomas in all patients as wells between groups 1 and 2 were not significant. In group 2,he axial length of eyes with type IX staphylomas wasignificantly longer than eyes with types I and II staphy-omas (P � .03 and .007, respectively).

MYOPIC FUNDUS LESIONS AND GRADES OR TYPES OF

OSTERIOR STAPHYLOMA: Eyes classified as M1, M2,nd M3, were categorized as having mild myopic retinalegeneration, and eyes classified as M4 and M5 wererouped as having severe myopic degeneration (Table 1).n group 1, 24 (27.3%) of 88 eyes had severe myopicegeneration, and in group 2, 71 (58.7%) of 121 eyes had

TABLE 2. Grades of Posterior Staphylom

Grades

Total

No. (%) Axial Length (mm) No. (%

0 21 eyes (10.0) 27.0 � 1.13 17 eye

1 119 eyes (56.9) 29.0 � 1.68 64 eye

2 45 eyes (21.5) 29.9 � 1.57 Seven eye

3 23 eyes (11.0) 29.7 � 1.28

4 One eye (0.5) 31.3

The prevalence of grade 2 staphyloma was significantly higher in

TABLE 3. Types of Posterior Staphylom

Types

Total

No. (%) Axial Length (mm) No. (%

I 44 eyes (23.4) 29.1 � 1.92 13 eyes (1

II 99 eyes (52.7) 29.2 � 1.64 48 eyes (6

III 8 eyes (4.3) 27.5 � 1.20 6 eyes (8

IV 0 — 0

V 5 eyes (2.7) 29.1 � 0.18 3 eyes (4

VI 0 — 0

VII 0 — 0

VIII 0 — 0

IX 32 eyes (17.0) 30.1 � 1.63 1 eye (1

X 0 — 0

evere myopic degeneration (Table 1). This difference was (


tatistically significant (P � .0001). CNV was detected in5 eyes (17.0%) in group 1 and in 28 eyes (23.1%) inroup 2. This difference was not statistically significant.

The relationships between myopic fundus lesions andhe grade of the posterior staphyloma are summarized inigure 3 and Table 4. Overall, our data showed that theigher the grade of the posterior staphyloma, the moreevere the retinal degeneration tended to be (Figure 3).one of the eyes with grade 0 staphyloma had severe

egeneration (M4 and M5), but 42.8% with grade 1taphyloma had severe degeneration, 62.2% with grade 2taphyloma had severe degeneration, 69.6% with grade

staphyloma had severe degeneration, and 100% withrade 4 staphyloma had severe degeneration. Althoughhere was an increase in the prevalence of severe degen-ration with an increase in the depth of the staphyloma,he differences among grades 1, 2, and 3 did not reachtatistical significance. Because the patient age also mayffect the grade of the myopic degeneration, we examinedhe grades of myopic degeneration in group 1 and in group

separately. The results demonstrated that even in olderatients (group 2), the higher grades of posterior staphylomaere 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

n 44 eyes (21.1%), macular retinoschisis in 24 eyes

d Axial Length in Different Age Groups

p 1 (�50 yrs) Group 2 (� 50 yrs)

Axial Length (mm) No. (%) Axial Length (mm)

3) 27.2 � 1.19 4 eyes (3.3) 26.5 � 0.39

7) 29.0 � 1.73 55 eyes (45.5) 29.1 � 1.61

) 30.3 � 0.99 38 eyes (31.4) 29.8 � 1.66

— 23 eyes (26.1) 29.7 � 1.28

— One eye (0.8) 31.3

nts older than 50 years than in those younger than 50 years.

d Axial Length in Different Age Groups

p 1 (� 50 yrs) Group 2 (� 50 yrs)

Axial Length (mm) No. (%) Axial Length (mm)

28.8 � 1.54 31 eyes (26.5) 29.3 � 2.08

29.4 � 1.21 51 eyes (43.6) 29.0 � 1.54

26.9 � 0.71 2 eyes (1.7) 29.6 � 0.44

— 0 —

28.9 � 0.23 2 eyes (1.7) 29.3 � 0.15

— 0 —

— 0 —

— 0 —

30.5 31 eyes (26.5) 30.3 � 1.62

— 0 —

a an

Grou

)

s (19.

s (72.

s (8.0

0

0

a an

Grou

)

8.3)

7.6)

.5)

.2)

.4)

11.5%), and macular holes in six eyes (2.9%) among all of


tlwd1nwoolsd

w3h1

tThste7demspwTel

ebs

rcwq(

●

FtooittaplTepbf

taesr

O

ilpyyeeopd

hyittet

Fgght

1

he 209 eyes. None of these types of lesion, that is, CNV,acquer cracks, macular retinoschisis, and macular holes,as detected in eyes with grade 0 staphyloma. A CNV wasetected in approximately 20% of the patients with gradeto 3 staphyloma, although the prevalence of CNVs was

ot significantly different among grades 1 to 3. Even whene examined the prevalence of the active phase of CNVnly, there was no significant difference in the prevalencef active CNV among grades 1 to 3. The prevalence ofacquer cracks tended to increase as the grade of thetaphyloma increased from grade 1 to 3, although theifferences were not significant.Statistical analysis showed that macular retinoschisis

as present significantly more frequently in eyes with gradestaphyloma than in eyes with grade 1 (P � .03). Macularoles were detected in only one to three eyes among gradesto 3.The distribution of the myopic fundus lesions and the

ypes of posterior staphyloma is shown in Figure 4 andable 5. Fifty percent of the eyes with type I staphylomaad severe retinal degeneration, 46.5% of eyes with type IItaphyloma had severe degeneration, 50% of eyes withype III staphyloma had severe degeneration, none of theyes with type V staphyloma had severe degeneration, and1.9% of the eyes with type IX staphyloma had severeegeneration. Statistical analysis demonstrated that theyes with type IX staphyloma had significantly more severeyopic retinal degeneration than those with type II

taphyloma (P � .01). However, the difference in therevalence of severe myopic retinal degeneration in eyesith type I and type IX staphylomas was not significant.he prevalence of severe myopic retinal degeneration inyes with type I and type II staphyloma was significantly

IGURE 3. Bar graph demonstrating the frequency of differentrades of myopic degeneration as a function of the differentrades of posterior staphyloma. The data showed that theigher the grade of the posterior staphyloma, the more severehe myopic retinal degeneration tended to be.

ower than in eyes with type IX staphyloma (P � .02). We p


xcluded types III and V from the statistical analysesecause the macular area was not included within thetaphylomatous area in these two types.

The prevalence of CNVs, active CNVs, and macularetinoschisis were not significantly different among eyeslassified as types I, II, and IX staphylomas. However, eyesith lacquer cracks were detected significantly more fre-uently in eyes with type IX compared with type I staphylomaP � .03) as well as with type II staphylomas (P � .001).

LONG-TERM CHANGES IN POSTERIOR STAPHYLOMAS:

ifteen eyes of nine patients were followed up for morehan 20 years in our high myopia clinic. The clinical dataf these nine patients are summarized in Table 6. The typef posterior staphyloma was determined by binocularndirect ophthalmoscopy at each follow-up examination byhree or more ophthalmologists. At the initial examina-ion, a posterior staphyloma was detected in 10 of 15 eyes,nd all were classified as type II. Three eyes of threeatients showed a change from type II to type IX staphy-oma at 17 years (Case 1 in Table 6), 15 years (Case 2 inable 6), and 18 years (Case 3 in Table 6) after the initialxamination (Figure 5). In these patients, a ridge-likerotrusion developed temporal to the optic disk at agesetween their late 40s through the early 50s and trans-ormed the staphyloma to type IX.

In these three eyes that showed the progression of theype of staphyloma, a progression of myopic degenerationlso was observed (Table 6). In contrast, in the other 12yes that did not show a change of the type of the posteriortaphyloma, only two eyes showed a progression of myopicetinal degeneration.

DISCUSSION

UR RESULTS SHOWED THAT A STAPHYLOMA WAS PRESENT

n 90% of the patients with high myopia, and the preva-ence of staphylomas was significantly higher in olderatients (96.7% in those 50 years of age and older) than inounger patients (80.7% in patients younger than 50ears). Stiedl and Pruett10 reported that 88 (75.9%) of 116yes had a posterior staphyloma; however, they analyzedyes with myopia ranging from �3 to �38 D with a meanf �14 D. Thus, it is difficult to compare the prevalence ofosterior staphylomas between the two studies, because theefinition of myopia was different.The prevalence of grade 2 staphyloma was significantly

igher in patients older than 50 years than in thoseounger than 50 years. This indicates that not only thencidence of posterior staphyloma but also the depth ofhe staphyloma increased as the patient ages. Interestingly,he axial length was not significantly different betweenyes with grade 1 to 3 staphyloma. However, if we followhe changes in the grade of staphyloma in the same
atient, it may be expected that the axial length would

iHwiww

iweof

oahtlg2ptns

liptrdydptiioos

itgsfhp

Fgtfdst

ylom

V

ncrease with an increase in the grade of staphyloma.owever, this was not found, probably because there was aide range of axial lengths in eyes with a staphyloma at the

nitial examination. Curtin also reported an unusuallyide range of refractive errors and axial lengths for eyesith the same type of staphyloma.9

The type II staphylomas were the most prominent typen groups 1 and 2. In contrast, Curtin reported that type Ias the most prominent and was observed in 55% of theyes with a posterior staphyloma, and the type II wasbserved in only 8.4% of the eyes examined (calculated

IGURE 4. Bar graph demonstrating the frequency of differentrades of myopic degeneration as a function of the differentypes of posterior staphyloma. The data showed that therequency of the grade of myopic degeneration varied among theifferent types of staphylomas; however, eyes with type IXtaphyloma had more severe myopic retinal degeneration thanhose with type II staphyloma.

TABLE 4. The Relationship between Myopic F

Variables Grade 0 (21 Eyes) Grade 1 (119

Choroidal neovascularization 0 eyes (0%) 27 eyes (2

Choroidal neovascularization

(active phase) 0 eyes (0%) Six eyes (5

Lacquer cracks 0 eyes (0%) 23 eyes (1

Macular retinoschisis 0 eyes (0%) 11 eyes (9

Macular holes 0 eyes (0%) One eye (0

Grades of myopic degeneration

M0 0 eyes (0%) 0 eyes (0

M1 21 eyes (100%) 0 eyes (0

M2 0 eyes (0%) 19 eyes (1

M3 0 eyes (0%) 49 eyes (4

M4 0 eyes (0%) 43 eyes (3

M5 0 eyes (0%) Eight eyes (6

The data showed that the higher the grade of the posterior staph

rom his Table II).9 Oie and associates examined the types c


f staphyloma in 28 Japanese with highly myopic eyes withmacular hole retinal detachment (MHRD) and in 47

ighly myopic eyes without an MHRD.12 They reportedhat in the eyes with an MHRD, 19% had type I staphy-oma and 63% had type II staphyloma, whereas in theroup without an MHRD, 43% had type I staphyloma and5% had type II staphyloma. Although the number of theiratients was much smaller, their results also indicated thathe prevalence of type II staphyloma was higher in Japa-ese patients than that reported by Curtin (who mainlytudied White persons).9

In group 2, the prevalence of type II staphylomas wasower than in group 1, and instead, type IX staphylomancreased. In type IX staphyloma, a ridge-like protrusion wasresent temporal to the optic disk. And more importantly, inhe patients who were followed up for more than 20 years, theidge-like protrusion developed in the three patients whoemonstrated the progression from type II to type IX staph-loma. These findings suggest that type IX staphylomasevelop secondarily by the development of a ridge-likerotrusion temporal to the optic disk in eyes originally withype II staphyloma as the patient ages. Therefore, our resultsndicated that the posterior staphyloma not only deepens, butts morphologic features also change as the patients growlder. This is important because these morphologic changesf the posterior staphyloma enhance the development ofevere myopic retinal degeneration.

The sclera is a typical connective tissue and consists ofnterwoven collagen fibrils in close association with pro-eoglycans. The number, arrangement, and types of colla-en fibrils are considered to determine the mechanicaltrength of a sclera. The reason why the morphologiceatures of posterior staphyloma worsen with increasing ageas not been clarified fully, and some authors have re-orted alterations in the composition of the sclera extra-

s Lesions and Grade of Posterior Staphyloma

Grade 2 (45 Eyes) Grade 3 (23 Eyes) Grade 4 (One Eye)

) 11 eyes (24.4%) Five eyes (21.7%) 0 eye (0%)

Two eyes (4.4%) One eye (4.3%) 0 eyes (0%)

) 13 eyes (28.9%) Eight eyes (34.8%) 0 eyes (0%)

Seven eyes (15.6%) Six eyes (26.1%) 0 eyes (0%)

Three eyes (6.7%) Two eyes (8.7%) 0 eyes (0%)

0 eyes (0%) 0 eyes (0%) 0 eyes (0%)

0 eyes (0%) 0 eyes (0%) 0 eyes (0%)

) Three eyes (6.7%) 0 eyes (0%) 0 eyes (0%)

) 14 eyes (31.1%) Seven eyes (30.4%) 0 eyes (0%)

) 17 eyes (37.8%) 12 eyes (52.2%) 0 eyes (0%)

11 eyes (24.4%) Four eyes (17.4%) One eye (100%)

a, the more severe the retinal degeneration tended to be.

undu

Eyes)

2.7%

.0%)

9.3%

.2%)

.8%)

%)

%)

6.0%

1.2%

6.1%

.7%)

ellular matrix in humans13,14 as well as animals.15


wabsrmnliwtmt

oofvamis

soew

(8.1%

1

Our results showed that the higher grades of staphylomaere associated with more severe myopic retinal degener-tion, which was similar to the results previously reportedy Stiedl and Pruett.10 Curtin and Karlin also reported atrong correlation between axial length and myopic cho-ioretinal atrophy, although the correlation between theyopic chorioretinopathy and posterior staphyloma wasot reported.16 Among the independent myopic macular

esions, the prevalence of macular retinoschisis was signif-cantly higher in eyes with grade 3 staphylomas comparedith those with grade 1 staphylomas. We have reported

hat macular retinoschisis was detected only in highlyyopic eyes with a posterior staphyloma,17 which supports

TABLE 5. The Relationship between Myopic F

Variables Type I (44 Eyes) Type II (99

Choroidal neovascularization Seven eyes (15.9%) 23 eyes

Choroidal neovascularization

(active phase) Two eyes (4.5%) Five eyes

Lacquer cracks 11 eyes (25%) 17 eyes

Macular retinoschisis Nine eyes (20.5%) Nine eyes

Macular holes Two eyes (4.5%) Two eyes


M0 0 eyes (0%) 0 eyes

M1 0 eyes (0%) 0 eyes

M2 Two eyes (4.5%) 15 eyes

M3 20 eyes (45.5%) 38 eyes

M4 10 eyes (22.7%) 38 eyes

M5 12 eyes (27.3%) Eight eyes

TABLE 6. Characteristics of Patients with Long-Term Follow-u

Patient

No. Sex Eye

At Initial Examination

Age

(yrs)

Refractive

Error (D)

Axial Length

(mm)

Type of

Staphyloma

Myopic

Degeneration*

1 F R 42 �22.0 31.9 II M4

2 F R 48 �20.0 31.8 II M3

L �13.0 29.0 II M3

3 F R 47 �9.0 27.8 II M2

4 F L 48 �13.0 29.0 II M3

5 F R 44 �19.0 28.4 II M3

L �15.0 27.9 II M3

6 F R 29 �14.0 28.8 II M3

L �16.0 29.3 II M3

7 M R 50 �14.0 27.2 0 M1

L �12.0 27.0 0 M1

8 F R 35 �11.0 29.7 0 M1

L �12.0 29.9 0 M1

9 M R 35 �23.0 30.9 II M2

L �11.0 29.1 0 M1

D � diopter; F � female; IOL � intraocular lens; L � left; M � m

*See Methods for classification.

he idea on the importance of staphylomas in the devel- r


pment of macular retinoschisis. Although the mechanismf macular retinoschisis development has not been clarifiedully, some causative factors such as the presence ofascular microfolds,18 paravascular inner lamellar hole,19

nd subsequent tractional detachment of inner limitingembrane20 have been suggested. An increased mechan-

cal tension caused by an increased depth of posteriortaphyloma may facilitate these proposed causative factors.

Stiedl and Pruett10 reported that the eyes with thehallowest staphyloma (grade 1) had the highest frequencyf CNV. They suggested that it is possible that the grade 1yes may be healthier and more metabolically active withell-perfused chorioretinal tissue and good capacity to

s Lesions and Type of Posterior Staphyloma

Type III (8 Eyes) Type V (5 Eyes) Type IX (32 Eyes)

) Three eyes (37.5%) 0 eyes (0%) 10 eyes (31.3%)

) 0 eyes (0%) 0 eyes (0%) Two eyes (6.3%)

) 0 eyes (0%) 0 eyes (0%) 16 eyes (50%)

) 0 eyes (0%) 0 eyes (0%) Six eyes (18.8%)

) 0 eyes (0%) 0 eyes (0%) Two eyes (6.3%)

0 eyes (0%) 0 eyes (0%) 0 eyes (0%)

0 eyes (0%) 0 eyes (0%) 0 eyes (0%)

) Three eyes (37.5%) One eyes (20%) Two eyes (6.3%)

) One eyes (12.5%) Four eyes (80%) Seven eyes (21.9%)

) Four eyes (50%) 0 eyes (0%) 19 eyes (59.4%)

) 0 eyes (0%) 0 eyes (0%) Four eyes (12.5%)

the Long-Term Change of the Type of Posterior Staphyloma

At Final ExaminationChange of

Type of

Staphyloma

Follow-up

(yrs)

Refractive

Error (D)

Axial Length

(mm)

Type of

Staphyloma

Myopic

Degeneration*

8.0 (IOL) 33.3 IX M5 Y 26

6.0 (IOL) 32.4 IX M4 Y 22

5.0 (IOL) 29.8 II M3 N

4.25 (IOL) 28.6 IX M3 Y 27

5.0 (IOL) 29.8 II M3 N 22

�19.0 29.7 II M4 N 22

�15.0 29.3 II M3 N

�18.0 29.9 II M3 N 29

�18.0 29.5 II M3 N

�15.0 28.0 0 M1 N 20

�15.0 27.6 0 M1 N

�11.0 30.6 0 M1 N 23

�12.5 30.8 0 M1 N

�23.0 33.8 II M3 N 23

�11.5 29.4 0 M1 N

� no; R � right; Y � yes.

undu

Eyes)

(23.2%

(5.1%

(17.2%

(9.1%

(2.0%

(0%)

(0%)

(15.2%

(38.4%

(38.4%

p and

Age

(yrs)

68 �

70 �

�

74 �

70 �

66

49

70

58

58

ale; N

espond to injury by neovascular ingrowth. In contrast, the


pdsehtn

httsWtttslsccli

wpc

pptstodlir

pttishpptttsaa

Ttoca

F(s(op

V

revalence of CNV (total CNV and active CNV) was notifferent among different grades of staphylomas in ourtudy. The reason for this discrepancy is not clear; how-ver, one reason may be a difference in the classification ofigh myopia (� �3.0 D vs � �8.0 D). Thus, it is possiblehat some of the CNVs in their study may have beenonmyopic in origin (e.g., idiopathic CNV).Our results showed that eyes with type IX staphylomas

ad severe myopic retinal degeneration more frequentlyhan eyes with type II staphylomas (Table 5). In addition,he axial length of eyes with type IX staphyloma wasignificantly longer than those with type II staphyloma.

e suggest that there is an increase in the mechanicalension on the posterior pole as well as on the optic disk byhe ridge-like protrusion in eyes of type IX staphyloma andhat this probably facilitates the development and progres-ion of myopic retinal degeneration. The prevalence ofacquer cracks was significantly higher in eyes with type IXtaphyloma than in those with type II staphyloma. Lacquerracks are mechanical ruptures of the Bruch membraneaused by an axial elongation; therefore, an increased preva-ence of lacquer cracks in eyes with type IX may reflect anncreased mechanical expansion of the posterior fundus.

One of the most interesting aspect of our study was thate were able to examine the morphologic features of theosterior staphyloma in 15 eyes of nine patients periodi-

IGURE 5. Fundus photographs showing the progression fromLeft) Right fundus of a 42-year-old woman. Refractive errortaphyloma is visible (arrowheads), and the posterior fundus sRight) Twenty-six years later, the axial length of the same eyeptic disk (arrows), and the type of staphyloma has progressedosterior fundus shows a bare sclera appearance. The optic dis

ally for more than 20 years. The results showed the clear s

nd data collection (H.W.H., K.O.-M., N.S., K.H., M.M., T.Y.); review and app


rogression from type II to type IX staphyloma in threeatients. Our longitudinal study showed that all three ofhe eyes that showed a progression from type II to type IXtaphyloma had a progression of myopic retinal degenera-ion, whereas only two of 12 eyes without the progressionf the staphyloma showed a progression of the retinalegeneration. These findings indicate that the morpho-ogic changes of the posterior staphyloma may be moremportant for the development or progression of myopicetinal degeneration than the axial length alone.

In conclusion, we examined the grades and types ofosterior staphyloma in a large number of Japanese pa-ients with pathologic myopia. The results demonstratedhat the type II staphyloma was the most prominent typen Japanese patients with high myopia. The grade oftaphyloma and prevalence of type IX staphyloma wasigher in older patients. These findings suggest that theosterior staphyloma not only deepens but also its mor-hologic features change as the patients age, even thoughhe axial length does not change significantly. The longi-udinal study revealed a clear progression from type II toype IX staphyloma in three of 15 patients. The progres-ion to type IX staphyloma may be an important featurend may increase the mechanical tension on the macularrea and optic disk, which may cause the progression to

II to type IX staphyloma (right fundus of Case 1 in Table 6).�22.0 diopters and the axial length was 31.9 mm. Type II

s fibrovascular tissue (arrow) and focal chorioretinal atrophy.33.3 mm. A ridge-like protrusion can be seen temporal to the

ype IX. Focal chorioretinal atrophy has spread widely and theo is stretched vertically.

evere myopic retinal degeneration.

HIS STUDY WAS SUPPORTED IN PART BY RESEARCH GRANTS 16390495, 17591823, AND 19390441 FROM THE JAPAN SOCIETY FORhe Promotion of Science, Tokyo, Japan. The authors indicate no financial conflict of interest. Involved in design of study (H.W.H., K.O.-M.); conductf 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.);ritical 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.);

typewas

howwasto t

k als

roval of manuscript (K.O.M., T.T., M.M.) . Because the ultrasonography


tIp

a

1

1

1

o measure the axial length and to evaluate the morphologic features of posterior staphyloma is performed routinely for highly myopic patients, thenstitutional Review Board of the Tokyo Medical and Dental University determined that no approval to perform the examination is necessary. Therocedures 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 studynd for the revision of the final manuscript.

1

1

1

1

1

1

1

1

2

REFERENCES

1. Ghafour IM, Allan D, Foulds WS. Common causes ofblindness and visual handicap in the west of Scotland. Br JOphthalmol 1983;67:209–213.

2. Wong TY, Foster PJ, Hee J, et al. Prevalence and risk factorsfor refractive errors in adult Chinese in Singapore. InvestOphthalmol Vis Sci 2000;41:2486–2494.

3. Sperduto RD, Seigel D, Roberts J, et al. Prevalence of myopiain the United States. Arch Ophthalmol 1983;101:405–407.

4. Xu L, Wang Y, Li Y, et al. Causes of blindness and visualimpairment in urban and rural areas in Beijng. The BeijingEye 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 staphylo-matous sclera of high myopia: an electron microscopic study.Arch Ophthalmol 1979;97:912–915.

7. McBrien NA, Norton TT. Prevention of collagen crosslink-ing increases form deprivation myopia in tree shrew. Exp EyeRes 1994;59:475–486.

8. Pruett RC. Complications associated with posterior staphy-loma. Curr Opin Ophthalmol 1998;9:16–22.

9. Curtin BJ. The posterior staphyloma of pathologic myopia.Trans Am Ophthal Soc 1977;75:67–86.

0. Steidl SM, Pruett RC. Macular complications associatedwith posterior staphyloma. Am J Ophthalmol 1997;123:181–187.

1. Avila MP, Weiter JJ, Jalkh AE, et al. Natural history ofchoroidal neovascularization in degenerative myopia. Oph-
thalmology 1984;91:1573–1581.

2. Oie Y, Ikuno Y, Fujikado T, Tano Y. Relation of posteriorstaphyloma in highly myopic eyes with macular holeand retinal detachment. Jpn J Ophthalmol 2005;49:530 –532.

3. Dunlevy JR, Summers Rada JA. Interaction of lumican withaggrecan in the aging human sclera. Invest Ophthalmol VisSci 2004;45:3849–3856.

4. Rada JA, Achen VR, Penugonda S, Schmidt RW, MountBA. Proteoglycan composition in the human sclera duringgrowth and aging. Invest Ophthalmol Vis Sci 2000;41:1639–1648.

5. Albon J, Farrant S, Akhtar S, et al. Connective tissuestructure of the tree shrew optic nerve and associated agingchanges. Invest Ophthalmol Vis Sci 2007;48:2134–2144.

6. Curtin BJ, Karlin DB. Axial length measurements and funduschanges of the myopic eye. Am J Ophthalmol 1971;71:42–53.

7. Baba T, Ohno-Matsui K, Futagami S, et al. Prevalence andcharacteristics of foveal retinal detachment without macularhole in high myopia. Am J Ophthalmol 2003;135:338–342.

8. Sayanagi K, Ikuno Y, Gomi F, Tano Y. Retinal vascularmicrofolds in highly myopic eyes. Am J Ophthalmol 2005;139:658–663.

9. Shimada N, Ohno-Matsui K, Nishimuta A, et al. Detectionof paravascular lamellar holes and other paravascular abnor-malities by optical coherence tomography in eyes with highmyopia. Ophthalmology 2008;115:708–717.

0. Sayanagi K, Ikuno Y, Tano Y. Tractional internal limitingmembrane detachment in highly myopic eyes. Am J Oph-
thalmol 2006;142:850–852.

HMs

V

Biosketch

uang Wei Hsiang, MD, graduated from Osaka University Medical School in 1999, and has been working at Tokyoedical and Dental University since 2002. Dr Hsiang’s interest is on the development and progression of posterior

taphyloma in pathologic myopia.

POSTERIOR STAPHYLOMA IN PATHOLOGIC MYOPIAOL. 146, NO. 1 110.e1

1

SUPPLEMENTAL TABLE 1. The Relationship Between Grades of Myopic Degeneration and Grade of Posterior Staphyloma inGroup 1

Variables Grade 0 (21 Eyes) Grade 1 (119 Eyes) Grade 2 (45 Eyes) Grade 3 (23 Eyes) Grade 4 (one Eye)


M0 0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%) 0 eyes (0%)


M2 0 eyes (0%) 19 eyes (16%) Three eyes (6.7%) 0 eyes (0%) 0 eyes (0%)

M3 0 eyes (0%) 49 eyes (41.2%) 14 eyes (31.1%) Seven eyes (30.4%) 0 eyes (0%)

M4 0 eyes (0%) 43 eyes (36.1%) 17 eyes (37.8%) 12 eyes (52.2%) 0 eyes (0%)

M5 0 eyes (0%) Eight eyes (6.7%) 11 eyes (24.4%) Four eyes (17.4%) One eye (100%)

Depths of grade 1 staphyloma, � 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 inGroup 2

Variables Grade 0 (21 Eyes) Grade 1 (119 Eyes) Grade 2 (45 Eyes) Grade 3 (23 Eyes) Grade 4 (One Eye)




M2 0 eyes (0%) 19 eyes (16%) Three eyes (6.7%) 0 eyes (0%) 0 eyes (0%)

M3 0 eyes (0%) 49 eyes (41.2%) 14 eyes (31.1%) Seven eyes (30.4%) 0 eyes (0%)

M4 0 eyes (0%) 43 eyes (36.1%) 17 eyes (37.8%) 12 eyes (52.2%) 0 eyes (0%)

M5 0 eyes (0%) Eight eyes (6.7%) 11 eyes (24.4%) Four eyes (17.4%) One eye (100%)

Depths of grade 1 staphyloma, � 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).

AMERICAN JOURNAL OF OPHTHALMOLOGY10.e2 JULY 2008

Documents

Clinical Characteristics of Posterior Staphyloma in Eyes with Pathologic Myopia