ultrasound biomicroscopic study of ciliary body thickness in eyes with narrow angles

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Ultrasound Biomicroscopic Study of Ciliary Body Thickness in Eyes With Narrow Angles TAKASHI GOHDO, MD, TOYOAKI TSUMURA, MD, HIROYUKI IIJIMA, MD, KENJI KASHIWAGI, MD, AND SHIGEO TSUKAHARA, MD PURPOSE: To determine the ciliary body thickness and other biometric findings in eyes with narrow angles. METHODS: Eighteen otherwise normal eyes with nar- row angles in 18 Japanese patients and 18 normal control eyes with open angles in 18 age-matched and sex- matched Japanese patients were studied. A-scan ultra- sonography was performed to measure anterior chamber depth, lens thickness, axial length, and relative lens position. Ultrasound biomicroscopy was also performed to obtain measurements of the anterior ocular structures, including anterior chamber depth and ciliary body thick- ness at sites 1 mm and 2 mm posterior to the scleral spur (positions 1 and 2, respectively). RESULTS: Compared with normal control eyes, the narrow-angle eyes showed a shallower anterior chamber (narrow angle, 1.87 6 0.27 mm; control, 2.69 6 0.26 mm; P < .0001), a thicker lens (4.97 6 0.49 mm, 4.26 6 0.53 mm; P < .0001), a more anteriorly located lens (2.21 6 0.13, 2.35 6 0.14; P < .0001), a shorter axial length (22.70 6 0.97 mm, 23.41 6 0.86 mm; P 5 .012), and a thinner ciliary body (position 1: 454 6 107 mm, 602 6 86 mm; P < .0001; position 2: 203 6 50 mm, 321 6 68 mm; P < .0001). Lens thickness was significantly correlated with ciliary body thickness at positions 1 (R 2 5 0.34; P 5 .0001) and 2 (R 2 5 0.43; P < .0001). Anterior chamber depth was significantly correlated with ciliary body thickness at positions 1 (R 2 5 0.48; P < .0001) and 2 (R 2 5 0.56; P < .0001). CONCLUSION: Thinning of the ciliary body may be one of the important factors associated with the anterior location of the lens, the increased lens thickness, and the decreased anterior chamber depth in eyes with a narrow angle. (Am J Ophthalmol 2000;129:342–346. © 2000 by Elsevier Science Inc. All rights reserved.) A NGLE-CLOSURE GLAUCOMA THAT USUALLY DEVEL- ops in eyes with narrow angles is closely related to the depth of the anterior chamber, which is mainly determined by the lens position and thickness. Compared with normal eyes, eyes with primary angle-closure glau- coma show increased lens thickness 1–9 and a more anteri- orly situated lens, 1–3,7–10 the latter of which may be associated with anteriorly situated ciliary processes. 3,10 Ultrasound biomicroscopy, a new diagnostic procedure that provides high-quality images of the anterior segments of an eye, 9,11 has shown forward rotation of the ciliary body in eyes with primary angle-closure glaucoma in a previous study. 9 Because smooth muscles in the human ciliary body show an atrophic change with age on histologic examina- tion, 12 we hypothesized that the age-related atrophy of the ciliary body might be the cause of the anterior rotation of the ciliary processes, which is followed by a shallow anterior chamber and narrowing of the anterior chamber angle. In the present study, we made biometric measure- ments by means of ultrasound biomicroscopy and A-scan ultrasonography, including ciliary body thickness, in nar- row-angle eyes and normal eyes. PATIENTS AND METHODS EIGHTEEN EYES, WITH NARROW ANTERIOR CHAMBER AN- gles, of 18 Japanese subjects whose mean 6 SD age was 73 6 8 years (range, 60 – 85 years) were studied. Six eyes were fellow eyes of patients with acute angle-closure glaucoma. The remaining 12 randomly chosen eyes were from 12 patients in whom a shallow anterior chamber was noted incidentally. They were referred to us because of suspicion of developing angle-closure glaucoma, although they had never experienced blurred vision, haloes, or periocular pain. The male-to-female ratio was 4:14. All 18 eyes had gonioscopic results showing grade 0 to 2 angle depths in the Shaffer Accepted for publication Sept 8, 1999. From the Department of Ophthalmology, Yamanashi Medical Univer- sity, Tamaho, Yamanashi, Japan. This study was supported by Grant-in-Aid for Scientific Research (A) 10770924 from the Ministry of Education, Science, and Culture of the Japanese Government, Tokyo, Japan. Reprint requests to Shigeo Tsukahara, MD, Department of Ophthal- mology, Yamanashi Medical University, Tamaho, Yamanashi, 409-3898 Japan; fax: 81-552-73-6757; e-mail: [email protected] © 2000 BY ELSEVIER SCIENCE INC.ALL RIGHTS RESERVED. 342 0002-9394/00/$20.00 PII S0002-9394(99)00353-0

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Page 1: Ultrasound biomicroscopic study of ciliary body thickness in eyes with narrow angles

Ultrasound Biomicroscopic Studyof Ciliary Body Thickness

in Eyes With Narrow Angles

TAKASHI GOHDO, MD, TOYOAKI TSUMURA, MD, HIROYUKI IIJIMA, MD,KENJI KASHIWAGI, MD, AND SHIGEO TSUKAHARA, MD

● PURPOSE: To determine the ciliary body thickness andother biometric findings in eyes with narrow angles.● METHODS: Eighteen otherwise normal eyes with nar-row angles in 18 Japanese patients and 18 normal controleyes with open angles in 18 age-matched and sex-matched Japanese patients were studied. A-scan ultra-sonography was performed to measure anterior chamberdepth, lens thickness, axial length, and relative lensposition. Ultrasound biomicroscopy was also performedto obtain measurements of the anterior ocular structures,including anterior chamber depth and ciliary body thick-ness at sites 1 mm and 2 mm posterior to the scleral spur(positions 1 and 2, respectively).● RESULTS: Compared with normal control eyes, thenarrow-angle eyes showed a shallower anterior chamber(narrow angle, 1.87 6 0.27 mm; control, 2.69 6 0.26mm; P < .0001), a thicker lens (4.97 6 0.49 mm,4.26 6 0.53 mm; P < .0001), a more anteriorly locatedlens (2.21 6 0.13, 2.35 6 0.14; P < .0001), a shorteraxial length (22.70 6 0.97 mm, 23.41 6 0.86 mm; P 5.012), and a thinner ciliary body (position 1: 454 6 107mm, 602 6 86 mm; P < .0001; position 2: 203 6 50mm, 321 6 68 mm; P < .0001). Lens thickness wassignificantly correlated with ciliary body thickness atpositions 1 (R2 5 0.34; P 5 .0001) and 2 (R2 5 0.43;P < .0001). Anterior chamber depth was significantlycorrelated with ciliary body thickness at positions 1(R2 5 0.48; P < .0001) and 2 (R2 5 0.56; P < .0001).● CONCLUSION: Thinning of the ciliary body may be oneof the important factors associated with the anteriorlocation of the lens, the increased lens thickness, andthe decreased anterior chamber depth in eyes with a

narrow angle. (Am J Ophthalmol 2000;129:342–346.© 2000 by Elsevier Science Inc. All rights reserved.)

A NGLE-CLOSURE GLAUCOMA THAT USUALLY DEVEL-

ops in eyes with narrow angles is closely related tothe depth of the anterior chamber, which is mainly

determined by the lens position and thickness. Comparedwith normal eyes, eyes with primary angle-closure glau-coma show increased lens thickness1–9 and a more anteri-orly situated lens,1–3,7–10 the latter of which may beassociated with anteriorly situated ciliary processes.3,10

Ultrasound biomicroscopy, a new diagnostic procedurethat provides high-quality images of the anterior segmentsof an eye,9,11 has shown forward rotation of the ciliary bodyin eyes with primary angle-closure glaucoma in a previousstudy.9 Because smooth muscles in the human ciliary bodyshow an atrophic change with age on histologic examina-tion,12 we hypothesized that the age-related atrophy of theciliary body might be the cause of the anterior rotation ofthe ciliary processes, which is followed by a shallowanterior chamber and narrowing of the anterior chamberangle. In the present study, we made biometric measure-ments by means of ultrasound biomicroscopy and A-scanultrasonography, including ciliary body thickness, in nar-row-angle eyes and normal eyes.

PATIENTS AND METHODS

EIGHTEEN EYES, WITH NARROW ANTERIOR CHAMBER AN-

gles, of 18 Japanese subjects whose mean 6 SD age was 73 68 years (range, 60–85 years) were studied. Six eyes werefellow eyes of patients with acute angle-closure glaucoma.The remaining 12 randomly chosen eyes were from 12patients in whom a shallow anterior chamber was notedincidentally. They were referred to us because of suspicion ofdeveloping angle-closure glaucoma, although they had neverexperienced blurred vision, haloes, or periocular pain. Themale-to-female ratio was 4:14. All 18 eyes had gonioscopicresults showing grade 0 to 2 angle depths in the Shaffer

Accepted for publication Sept 8, 1999.From the Department of Ophthalmology, Yamanashi Medical Univer-

sity, Tamaho, Yamanashi, Japan.This study was supported by Grant-in-Aid for Scientific Research (A)

10770924 from the Ministry of Education, Science, and Culture of theJapanese Government, Tokyo, Japan.

Reprint requests to Shigeo Tsukahara, MD, Department of Ophthal-mology, Yamanashi Medical University, Tamaho, Yamanashi, 409-3898Japan; fax: 81-552-73-6757; e-mail: [email protected]

© 2000 BY ELSEVIER SCIENCE INC. ALL RIGHTS RESERVED.342 0002-9394/00/$20.00PII S0002-9394(99)00353-0

Page 2: Ultrasound biomicroscopic study of ciliary body thickness in eyes with narrow angles

classification without goniosynechia. Slit-lamp examinationshowed no abnormal findings except for shallow anteriorchambers and mild lens opacity. Intraocular pressures rangedfrom 12 to 18 mm Hg. Refractive errors were within 63diopters. The best-corrected visual acuity ranged from 20/40to 20/20. No eye had received antiglaucoma medication.

Eighteen normal eyes of 18 age-matched and sex-matched Japanese patients were selected as normal controlsubjects from the outpatients seen for complaints of mildcataract. All eyes had grade 3 to 4 angle depths in theShaffer classification without goniosynechia. They showedno ocular abnormality except for mild opacity in thecrystalline lens. The best-corrected visual acuity, refrac-tion, and intraocular pressure ranged from 20/40 to 20/20,from 23 diopters to 11 diopter, and from 12 to 18 mm Hg,respectively. Informed consent was obtained from allnarrow-angle subjects and normal control subjects beforethe ultrasonographic tests were performed.

A-scan ultrasonography was performed with an AutoAxial Length Biometer AL-010 (Toyo Medical, Tokyo,Japan). The last four reliable measurements were averaged.The anterior chamber depth measurement 1 (between theanterior surface of the cornea and the anterior surface ofthe lens), the lens thickness, and the axial length wererecorded. The relative lens position is the relative positionof the center of the lens determined by adding the anteriorchamber depth to half the lens thickness and then dividingthe sum by the axial length.2 The relative lens positionvalue was multiplied by 10.9

Ultrasound biomicroscopy was performed with a UBM840 instrument (Humphrey-Zeiss, San Leandro, Califor-nia) with a 50-MHz transducer-probe. After surface anes-thesia was achieved with 0.4% benoxinate, an eye cupfilled with fluid coupling medium 2% methylcellulose wasapplied to the eyeball between the eyelids. Examinationwas performed under room light. Each patient was in-structed to look at a fixation target placed on the ceiling toavoid the effects of accommodation. An image through the

center of the pupil was recorded for anterior chamberdepth measurement 2 (measured from the corneal endo-thelium to the anterior lens surface).9,11,13 The ciliary bodythickness was measured on the image of a meridionalsection at the valley between ciliary processes at thetemporal limbus in each eye. Fine movements of theultrasound biomicroscopy probe were required to explorethe areas of interest, always perpendicular to the surface ofthe eyeball. The measurement was performed with the instru-ment’s caliper software package. The thickness of the ciliarybody at positions 1 and 2 mm posterior to the scleral spur wasmeasured (positions 1 and 2, respectively) (Figure 1).

Intraobserver reproducibility is high for various ultrasoundbiomicroscopy measurements.11 In our study, a single well-trained observer (T.G.) performed all the ultrasound biomi-croscopy studies. The coefficients of variation were 0.2 foranterior chamber depth, 1.4 for ciliary body thickness atposition 1, and 2.2 for ciliary body thickness at position 2.

Statistical analyses were completed with SPSS for Win-dows (Version 6.13; SPSS Japan Inc, Tokyo, Japan). At test was used to compare each parameter of eyes withnarrow angles and normal eyes. Correlations betweenciliary body thickness (positions 1 and 2) and anteriorchamber depth (measurement 2) or lens thickness weretested by linear regression analysis and analysis of variance.Anterior chamber depth measurement 2, which is the trueanterior chamber depth from the endothelial surface of thecornea to the anterior lens surface, was used for thestatistical analysis instead of measurement 1.

RESULTS

EXAMPLES OF ULTRASOUND BIOMICROSCOPY IMAGES OF A

narrow-angle eye and of a normal control eye are shown inFigure 2. The image in the narrow-angle eye shows a thinnerciliary body, a more anteriorly rotated ciliary process, andnarrower anterior chamber angle than in the normal eye.

FIGURE 1. Schematic illustration and ultrasound biomicroscopy image of the measurement of ciliary body thickness. Ciliary bodythickness was measured perpendicular to the inner surface of the sclera at 1 mm (CBT1, arrows) and 2 mm (CBT2, arrows)posterior to the scleral spur (S, arrow).

CILIARY BODY THICKNESS IN NARROW-ANGLE EYESVOL. 129, NO. 3 343

Page 3: Ultrasound biomicroscopic study of ciliary body thickness in eyes with narrow angles

The results of the A-scan biometric study are given inTable 1. Compared with normal control eyes, the narrow-angle eyes showed a shallower anterior chamber (measure-ment 1) (narrow angle, 2.51 6 0.30 mm; normal, 3.39 6 0.32mm; P , .0001), a thicker lens (4.97 6 0.49 mm, 4.26 6 0.53mm; P , .0001), a more anteriorly located lens (2.21 6 0.13,2.35 6 0.14; P , .0001), and a shorter axial length (22.70 60.97 mm, 23.41 6 0.86 mm; P 5 .012).

The results of the ultrasound biomicroscopy biometricstudy are given in Table 2. Compared with normal controleyes, the narrow-angle eyes showed a shallower anteriorchamber (measurement 2) (narrow angle, 1.87 6 0.27 mm;normal, 2.69 6 0.26 mm; P , .0001), a thinner ciliarybody measurement 1 mm from the scleral spur (454 6 107mm, 602 6 86 mm; P , .0001), and a thinner ciliary bodymeasurement 2 mm from the scleral spur (203 6 50 mm,321 mm 6 68 mm; P , .0001).

The lens thickness was significantly correlated with theciliary body thickness at 1 mm (R2 5 0.34; P 5 .0001) and2 mm (R2 5 0.43; P , .0001) from the scleral spur (Figure3). The anterior chamber depth (measurement 2) wassignificantly correlated with the ciliary body thickness at 1mm (R2 5 0.48; P , .0001) and 2 mm (R2 5 0.56; P ,.0001) from the scleral spur (Figure 4).

DISCUSSION

IN PREVIOUS BIOMETRIC STUDIES IN EYES WITH PRIMARY

angle-closure glaucoma, the lens was thicker and moreanteriorly positioned.1–3,6,10,14 However, eyes with primary

FIGURE 2. (Left) Ultrasound biomicroscopy image of a normal control eye. The ciliary body is thick: its thickness at 1 mmposterior to the scleral spur (left arrows) is 752 mm and at 2 mm (right arrows), 432 mm. The ciliary process is not anteriorlyrotated, and the angle is wide open. (Right) Ultrasound biomicroscopy image of an eye with a narrow angle. The ciliary body is verythin: its thickness at 1 mm posterior to the scleral spur (left arrows) is 428 mm and at 2 mm (right arrows), 209 mm. A ciliaryprocess is anteriorly rotated and the angle is slit-like.

TABLE 1. A-Scan Biometric Parameters in Eyes WithNarrow Angle and Normal Eyes

Biometric Parameter

Mean 6 SD

P Value

Narrow Angle

(n 5 18)

Normal Controls

(n 5 18)

Axial length (mm) 22.70 6 0.97 23.41 6 0.86 .012

Anterior chamber depth

(mm)

2.51 6 0.30 3.39 6 0.32 ,.0001

Lens thickness (mm) 4.97 6 0.49 4.26 6 0.53 ,.0001

Relative lens position 2.21 6 0.13 2.35 6 0.14 ,.0001

TABLE 2. Ultrasound Biomicroscopy Parameters in EyesWith Narrow Angle and Normal Eyes

Biometric Parameter

Mean 6 SD

P Value

Narrow

Angle

(n 5 18)

Normal

Controls

(n 5 18)

Anterior chamber depth

(mm)

1.87 6 0.27 2.69 6 0.26 ,.0001

Ciliary body thickness 1

(mm)

454 6 107 602 6 86 ,.0001

Ciliary body thickness 2

(mm)

203 6 50 321 6 68 ,.0001

AMERICAN JOURNAL OF OPHTHALMOLOGY344 MARCH 2000

Page 4: Ultrasound biomicroscopic study of ciliary body thickness in eyes with narrow angles

angle-closure glaucoma may have received some medicalintervention. Since antiglaucoma eyedrops often affect theciliary body thickness,15 we excluded eyes that had re-ceived antiglaucoma medications, both in narrow-angleeyes and in those of normal control subjects. The presentstudy confirmed that narrow-angle eyes without glaucomamedication show thicker and more anteriorly positionedlenses.

Rotation of the ciliary body may play a part in eyes with

primary angle-closure glaucoma.3,10 Marchini and associ-ates9 showed forward rotation of the ciliary processes ineyes with primary angle-closure glaucoma by means ofultrasound biomicroscopy. In the present study, we ob-served the anterior rotation of the ciliary processes in mostnarrow-angle eyes without glaucoma medication (Figure2), although this could not be demonstrated statistically.

The present study showed that the ciliary body wasthinner in narrow-angle eyes than in normal control eyes.

FIGURE 3. (Left) Linear regression analysis shows a significant relationship for all subjects (n 5 36) (R2 5 .34, P 5 .0001)between the ciliary body thickness at 1 mm from the scleral spur (CBT1) and lens thickness. The 95% confidence intervals (thinlines) of the slope are shown above and below the regression line. (Right) Linear regression analysis shows a significant relationship(R2 5 .43, P 5 .0001) between the ciliary body thickness at 2 mm from the scleral spur (CBT2) and lens thickness in the allsubjects. The 95% confidence intervals (thin lines) of the slope are shown above and below the regression line.

FIGURE 4. (Left) Linear regression analysis shows a significant relationship (R2 5 .48, P < .0001) between the ciliary bodythickness at 1 mm from the scleral spur (CBT1) and anterior chamber depth, measurement 2 (ACD2) in all subjects in this study(n 5 36). The 95% confidence intervals (thin lines) of the slope are shown above and below the regression line. (Right) Linearregression analysis shows a significant relationship (R2 5 .56, P < .0001) between the ciliary body thickness at 2 mm from thescleral spur (CBT2) and anterior chamber depth, measurement 2 (ACD2) in all subjects. The 95% confidence intervals (thin lines)of the slope are shown above and below the regression line.

CILIARY BODY THICKNESS IN NARROW-ANGLE EYESVOL. 129, NO. 3 345

Page 5: Ultrasound biomicroscopic study of ciliary body thickness in eyes with narrow angles

Also, the anterior chamber depth and the lens thicknessshowed a significant correlation with ciliary body thick-ness. Recent ultrasound biomicroscopy studies have shownthat the ciliary body effusion causes anterior rotation of theciliary processes, which is associated with a shallow ante-rior chamber and a narrowed angle in various diseases.16–21

Pavlin and associates16 stated that forward rotation of theciliary process swings the zonules and lens forward andcauses shallowing of the anterior chamber. Although theciliary body effusion was absent in the narrow-angle eyes inthe present study, their thin ciliary body may be thought tobe atrophied and cause anterior rotation of the ciliaryprocesses because the ciliary body that is firmly attached tothe scleral spur may prevent ciliary processes from anteriorrotation. Therefore, we speculated that the thinner ciliarybody may cause advancing and thickening of the lens andresultant narrow angle and shallow anterior chamberthrough anterior rotation of the ciliary processes andloosening of the zonules.

Eyes with primary angle-closure glaucoma show ashorter axial length than normal eyes in biometric stud-ies.2–10,14 In the present study, the axial length in narrow-angle eyes was shorter than that in normal eyes. Thinningof the ciliary body may be related to the presence ofanatomically smaller structures in a small eye.

Correlation between the ciliary body thickness and lensthickness and the anterior chamber depth was shown inthis study. In a histologic study of meridional sections ofthe human ciliary body, significant reduction of the area ofciliary muscle was shown with age.12 Because the crystal-line lens is continuously growing, lens thickness increaseswith age. Also, a small amount of anterior movement ofthe lens occurs in a human eye with age.22 The thinning ofthe ciliary body may be an age-related change associatedwith these age-related biometric findings of the anteriorsegment.

We have shown that the ciliary body of the narrow-angle eyes is thinner than that of normal control eyes andthat the thickness of the ciliary body is related to lensthickness and anterior chamber depth by means of ultra-sound biomicroscopy. Thinning of the ciliary body may beone of the important factors associated with anteriorlocation of lens, increased lens thickness, and the de-creased anterior chamber depth.

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2. Lowe RF. Aetiology of the anatomical basis for primaryangle-closure glaucoma: biometrical comparisons betweennormal eyes and eyes with primary angle-closure glaucoma.Br J Ophthalmol 1970;54:161–169.

3. Tomlinson A, Leighton DA. Ocular dimensions in theheredity of angle-closure glaucoma. Br J Ophthalmol 1973;57:475–486.

4. Clemmesen V, Luntz MH. Lens thickness and angle-closureglaucoma: a comparative oculometric study in South AfricanNegroes and Danes. Acta Ophthalmol 1976;54:193–197.

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AMERICAN JOURNAL OF OPHTHALMOLOGY346 MARCH 2000