- Email: [email protected]
Long anterior zonules and pigment dispersion
dures and decreases the postoperative blood– ocular barrier breakdown. Graefes Arch Clin Exp Ophthalmol 2002;240: 423–429. 2. Peyman GA, Cheema R, Conway MD, Fang T. Triamcinolone acetonide as an aid to visualization of the vitreous and the posterior hyaloid during pars plana vitrectomy. Retina 2000;20:554 –555. 3. Sakamoto T, Koga H, Noda Y, Ishibashi T. Optic disk cup filled with triamcinolone. Retina 2002;22:516 –518. 4. Enaida H, Sakamoto T, Ueno A, et al. Submacular deposition of triamcinolone acetonide after triamcinolone-assisted vitrectomy. Am J Ophthalmol 2003;135:243–246.
Long anterior zonules inserted onto the central lens capsule may cause mechanical disruption of the pigment epithelium at the pupillary ruff and central iris leading to pigment dispersion. (Am J Ophthalmol 2003;136:1176 –1178. © 2003 by Elsevier Inc. All rights reserved.)
CONCLUSIONS:
I
tion syndrome, pigment particles are liberated from iris pigment epithelium due to mechanical damage from iridozonular and iridolenticular friction, respectively. Here, we propose a new mechanism for liberation of pigment whereby elongated anterior zonules inserted centrally on the surface of the anterior lens capsule cause iris pigment epithelial injury and subsequent pigment release. Fifteen patients were examined by at least one of four authors at four different institutions (S.E.M., R.R., G.J.K., K.N-M.). The demographic and clinical findings are summarized in Table 1. Cases 1 to 7 were described in a pedigree with an autosomal dominant hemorrhagic macular dystrophy.1 Cases 8 to 15 were unrelated to this pedigree. Each patient had long anterior zonules extending toward the central visual axis (Figure 1A). Pigment along these elongated zonules was commonly visible (Figure 1B). No eyes had pseudoexfoliation or peripheral iris concavity, which was confirmed by ultrasound biomicroscopy (Paradigm Medical Industries, Inc., Salt Lake City, Utah, USA) in Patients 1 to 7 and 11. No other identifiable causes were noted for pigment liberation, such as anterior segment tumors, primary familial amyloidosis, uveitis, trauma, or iatrogenic pigment dispersion from intraocular surgery. Cases 1, 8, 10, 11, 12, and 14 were treated for glaucoma, and Case 3 was treated for elevated intraocular pressure. In Cases 1 to 9 and 15, the zonule-free zone of the anterior capsule was less than 4.5 mm. Normally, this zone is estimated to be 6.9 mm.2 Farnsworth and Shyne demonstrated an age-related increase in the zonule insertion to lens equator distance of ⬍1mm.3 This small shift is thought to be due to capsule turnover, with new capsule produced at the lens equator and the centrally located capsule reabsorbed. This proposed capsule turnover would lead to a centripetal zonule migration. This small shift does not explain the length of the zonules or the size of the zonule-free zone in our patients. A capsulorrhexis specimen obtained from Case 15 during cataract surgery showed a normal lens capsule, degenerated epithelium (Figure 2A), and ultrastructurally normal zonule lamellae remnants (Figure 2B). Pigmented granules and cellular debris were adherent to or embedded within the fibrillar layer of the zonule lamella (Figure 2, C and D). There was notable absence of exfoliation material. In summary, we described a case series with pigment dispersion and long anterior zonules. Previously, two patients with long anterior zonules were reported,4 but pigment dispersion was not described. It is possible that the “opacifications strie´ es coronaires superficielles du cristal-
Long Anterior Zonules and Pigment Dispersion Sayoko E. Moroi, MD, PhD, Kurt K. Lark, MD, Paul A. Sieving, MD, PhD, Kouros Nouri-Mahdavi, MD, Ursula Schlo¨ tzer-Schrehardt, PhD, Gregory J. Katz, MD, and Robert Ritch, MD PURPOSE: To describe pigment dispersion associated with long anterior zonules. DESIGN: Multicenter observational case series. METHODS: Fifteen patients, seven of whom were treated for glaucoma or ocular hypertension, were identified with long anterior zonules and pigment dispersion. Transmission electron microscopy was performed on one anterior capsule specimen. RESULTS: All patients had anterior zonules that inserted centrally on the lens capsule. Signs of pigment dispersion included corneal endothelial pigmentation, loss of the pupillary ruff, and variable trabecular meshwork pigmentation. Ultrasound biomicroscopy verified the lack of posterior iris insertion and concavity. There was no exfoliation material. Transmission electron microscopy showed zonular lamellae with adherent pigment granules, and no exfoliation material.
Accepted for publication June 11, 2003. From the Department of Ophthalmology and Visual Sciences, University of Michigan, Ann Arbor, Michigan (S.E.M., P.A.S.); Cabarrus Eye Center, Concord, North Carolina (K.K.L.); National Eye Institute, National Institutes of Health, Bethesda, Maryland (P.A.S.); Department of Ophthalmology, Iran University of Medical Sciences, Tehran, Iran (K.N-M.); Department of Ophthalmology, Jules Stein Eye Institute, Los Angeles, California (K.N-M.); Department of Ophthalmology, University Erlangen-Nu¨ rnberg, Erlangen, Germany (U.S-S.); St. Joseph Mercy Hospital, Ypsilanti, Michigan (G.J.K.); The New York Eye and Ear Infirmary, New York, and The New York Medical College, Valhalla, New York (R.R.). Research to Prevent Blindness Career Development Award, New York, NY (S.E.M.), Research to Prevent Blindness Senior Scientific Investigator Award (P.A.S.), and the Steven and Shelley Einhorn Research Fund of the New York Glaucoma Research Institute (R.R.). Presented at American Glaucoma Society, 13th Annual Meeting, March 6 –9, 2003, San Francisco, California. Inquiries to Sayoko E. Moroi, MD, PhD, Department of Ophthalmology & Visual Sciences, University of Michigan, 1000 Wall Street, Ann Arbor, MI 48105; fax: (734) 936-2340; e-mail: [email protected]
1176
AMERICAN JOURNAL
N PIGMENT DISPERSION SYNDROME (PDS) AND EXFOLIA-
OF
OPHTHALMOLOGY
DECEMBER 2003
TABLE 1. Demographics and Clinical Characteristics Age (Years)
Gender
Race
Vision
1
68
F
W
20/300 OU
2 3 4
41 72 46
M F F
W W W
20/15 OU 20/200 OU 20/15 OU
5
33
F
W
20/15 OU
6 7
65 40
F M
W W
20/300 OU 20/15 OU
8
80
F
B
20/25 OU
9
78
M
W
10 11
66 66
F M
W W
20/50 OD 20/100 OS 20/30 OU 20/20 OU
12
67
F
W
13
72
F
W
14
47
M
A
15
81
F
W
Case
20/60 OD 20/200 OS 20/400 OD 20/60 OD 20/200 OD 20/50 OS 20/60 OU
IOP (mm Hg)
Corneal Endopigment*
Mid-peripheral Iris TIDs
Pupillary Ruff
Zonular Free Zone (mm)
TM Pigment†
27 OD 21 OS 10 OU 21 OU 16 OD 17 OS 14 OU
KS OU
Present OD
TIDs OU
ⱕ3.5 OU
4
None OU None OU None OU
Absent OU Absent OU Absent OU
TIDs OU TIDs OU Normal OU
0 3 2
None OU
Absent OU
TIDs OU
KS OU None OU
Absent OU Absent OU
TIDs OU TIDs OU
DP OU
Absent OU
Not reported
KS OU
Absent OU
Normal OU
KS OU None OU
Absent OU Absent OU
Not reported Not reported
2.5 OU ⱕ3.0 OU 3.0 OD 3.1 OS 2.7 OD 3.0 OS ⱕ3.0 OU 3.0 OD 2.7 OS 2.5 OD 2.1 OS IOL OD 4.5 OS Not reported Not reported
None OU
Not reported
Not reported
“Star burst”
2
Not reported
Not reported
Present OU
Not reported
No gonio
Not reported
Not reported
Not reported
Not reported
3–4
None OU
Absent OU
TIDs OU
20 OU 15 OD 13 OS 24 OD 25 OS 13 OD 15 OS 20 OU low 20’s OU 22 OD 19 OS 16 OD 14 OS 30 OD 20 OS 13 OU
3.5 OU
2 3 1, patchy 1, patchy 2–3, patchy 3 2–3, patchy
2
F ⫽ female; M ⫽ male; W ⫽ white; B ⫽ black; A ⫽ Afghan; IOP ⫽ intraocular pressure; OD ⫽ right eye; OS ⫽ left eye; OU ⫽ both eyes; TID ⫽ transillumination defect. *Corneal endopigment was documented either as a Krukenberg spindle (KS), diffuse pattern (DP), or none. † TM ⫽ trabecular meshwork. Pigmentation grading system: 0 ⫽ none, 1 ⫽ faint, 2 ⫽ minimal, 3 ⫽ moderate, 4 ⫽ dense.
FIGURE 1. (A) Long anterior zonules were visible in all cases on the anterior capsule surface, which were apparent on direct illumination and retroillumination after pupillary dilation as in Case 1. (B) Pigment was commonly noted along some of the long anterior zonules as in Case 10.
lin”5 and “retro-iridial lines”6 may represent the same findings. Recently, the prevalence of pigmented lens striae was estimated at 1.8% in a black primary eyecare populaVOL. 136, NO. 6
tion.7 Our electron microscopy results suggest a mechanism of pigment release from the pigmented epithelium located at the pupillary ruff and the central iris, which are
BRIEF REPORTS
1177
FIGURE 2. Transmission electron microscopy of the anterior lens capsule in pigmented long anterior zonules (Case 15). (A) Overview showing a normal central anterior lens capsule, covered by an irregular zonule lamella, and a degenerative lens epithelium (bar is 5 m). (B) Detail of the zonule lamella showing a loose fibrillar substructure and merging with the superficial lens capsule (bar is 1 m). (C) Pigment granules and cell debris are embedded within the thickened zonule lamella (bar is 1 m). (D) Fragments of iris pigment epithelial cells adhere to the irregular zonule lamella (bar is 1 m).
in close proximity to the elongated zonules. The zonules appear normal because standard phacoemulsification did not indicate fragility (Cases 9 and 15). This mechanism is distinct from PDS, in which the iridozonular contact occurs between the midperipheral iris and anterior zonule bundles.8 Though subtle and easily missed on biomicroscopy, the long anterior zonules may be not uncommon but just not previously recognized as a distinct entity associated with pigment dispersion.
2. 3. 4. 5. 6.
ACKNOWLEDGMENTS
The electron micrograph montage was created with the assistance of Mr. Mitch Gillett.
7.
REFERENCES
8.
1. Ayyagari R, Griesinger IB, Bingham E, Lark KK, Moroi SE, Sieving PA. Autosomal dominant hemorrhagic macular dys-
1178
AMERICAN JOURNAL
OF
trophy not associated with the TIMP3 gene. Arch Ophthalmol 2000;118:85–92. Sakabe I, Oshika T, Lim SJ, Apple DJ. Anterior shift of zonular insertion onto the anterior surface of human crystalline lens with age. Ophthalmology 1998;105:295–299. Farnsworth PN, Shyne SE. Anterior zonular shifts with age. Exp Eye Res 1979;28:291–297. Koch DD, Liu JF. Zonular encroachment on the anterior capsular zonular-free zone. Am J Ophthalmol 1988;106:491–92. Abramowicz I. Opacifications strie´ es coronaires superficielles du cristallin. Ann D’Oculistique 1933;170:602–604. Berliner ML. Biomicroscopy of the eye, slit lamp microscopy of the living eye. New York: Paul B. Hoeber, Inc.; 1960: 1023–1024. Roberts DK, Lo PS, Winters JE, Castells DD, Alexander CC, Teitelbaum BA. Prevalence of pigmented lens striae in a black population: a potential indicator of age-related pigment dispersal in the anterior segment. Optom Vis Sci 2002;79:681– 687. Campbell DG. Pigmentary dispersion and glaucoma. A new theory. Arch Ophthalmol 1979;97:1667–1672.
OPHTHALMOLOGY
DECEMBER 2003
Long anterior zonules inserted onto the central lens capsule may cause mechanical disruption of the pigment epithelium at the pupillary ruff and central iris leading to pigment dispersion. (Am J Ophthalmol 2003;136:1176 –1178. © 2003 by Elsevier Inc. All rights reserved.)
CONCLUSIONS:
I
tion syndrome, pigment particles are liberated from iris pigment epithelium due to mechanical damage from iridozonular and iridolenticular friction, respectively. Here, we propose a new mechanism for liberation of pigment whereby elongated anterior zonules inserted centrally on the surface of the anterior lens capsule cause iris pigment epithelial injury and subsequent pigment release. Fifteen patients were examined by at least one of four authors at four different institutions (S.E.M., R.R., G.J.K., K.N-M.). The demographic and clinical findings are summarized in Table 1. Cases 1 to 7 were described in a pedigree with an autosomal dominant hemorrhagic macular dystrophy.1 Cases 8 to 15 were unrelated to this pedigree. Each patient had long anterior zonules extending toward the central visual axis (Figure 1A). Pigment along these elongated zonules was commonly visible (Figure 1B). No eyes had pseudoexfoliation or peripheral iris concavity, which was confirmed by ultrasound biomicroscopy (Paradigm Medical Industries, Inc., Salt Lake City, Utah, USA) in Patients 1 to 7 and 11. No other identifiable causes were noted for pigment liberation, such as anterior segment tumors, primary familial amyloidosis, uveitis, trauma, or iatrogenic pigment dispersion from intraocular surgery. Cases 1, 8, 10, 11, 12, and 14 were treated for glaucoma, and Case 3 was treated for elevated intraocular pressure. In Cases 1 to 9 and 15, the zonule-free zone of the anterior capsule was less than 4.5 mm. Normally, this zone is estimated to be 6.9 mm.2 Farnsworth and Shyne demonstrated an age-related increase in the zonule insertion to lens equator distance of ⬍1mm.3 This small shift is thought to be due to capsule turnover, with new capsule produced at the lens equator and the centrally located capsule reabsorbed. This proposed capsule turnover would lead to a centripetal zonule migration. This small shift does not explain the length of the zonules or the size of the zonule-free zone in our patients. A capsulorrhexis specimen obtained from Case 15 during cataract surgery showed a normal lens capsule, degenerated epithelium (Figure 2A), and ultrastructurally normal zonule lamellae remnants (Figure 2B). Pigmented granules and cellular debris were adherent to or embedded within the fibrillar layer of the zonule lamella (Figure 2, C and D). There was notable absence of exfoliation material. In summary, we described a case series with pigment dispersion and long anterior zonules. Previously, two patients with long anterior zonules were reported,4 but pigment dispersion was not described. It is possible that the “opacifications strie´ es coronaires superficielles du cristal-
Long Anterior Zonules and Pigment Dispersion Sayoko E. Moroi, MD, PhD, Kurt K. Lark, MD, Paul A. Sieving, MD, PhD, Kouros Nouri-Mahdavi, MD, Ursula Schlo¨ tzer-Schrehardt, PhD, Gregory J. Katz, MD, and Robert Ritch, MD PURPOSE: To describe pigment dispersion associated with long anterior zonules. DESIGN: Multicenter observational case series. METHODS: Fifteen patients, seven of whom were treated for glaucoma or ocular hypertension, were identified with long anterior zonules and pigment dispersion. Transmission electron microscopy was performed on one anterior capsule specimen. RESULTS: All patients had anterior zonules that inserted centrally on the lens capsule. Signs of pigment dispersion included corneal endothelial pigmentation, loss of the pupillary ruff, and variable trabecular meshwork pigmentation. Ultrasound biomicroscopy verified the lack of posterior iris insertion and concavity. There was no exfoliation material. Transmission electron microscopy showed zonular lamellae with adherent pigment granules, and no exfoliation material.
Accepted for publication June 11, 2003. From the Department of Ophthalmology and Visual Sciences, University of Michigan, Ann Arbor, Michigan (S.E.M., P.A.S.); Cabarrus Eye Center, Concord, North Carolina (K.K.L.); National Eye Institute, National Institutes of Health, Bethesda, Maryland (P.A.S.); Department of Ophthalmology, Iran University of Medical Sciences, Tehran, Iran (K.N-M.); Department of Ophthalmology, Jules Stein Eye Institute, Los Angeles, California (K.N-M.); Department of Ophthalmology, University Erlangen-Nu¨ rnberg, Erlangen, Germany (U.S-S.); St. Joseph Mercy Hospital, Ypsilanti, Michigan (G.J.K.); The New York Eye and Ear Infirmary, New York, and The New York Medical College, Valhalla, New York (R.R.). Research to Prevent Blindness Career Development Award, New York, NY (S.E.M.), Research to Prevent Blindness Senior Scientific Investigator Award (P.A.S.), and the Steven and Shelley Einhorn Research Fund of the New York Glaucoma Research Institute (R.R.). Presented at American Glaucoma Society, 13th Annual Meeting, March 6 –9, 2003, San Francisco, California. Inquiries to Sayoko E. Moroi, MD, PhD, Department of Ophthalmology & Visual Sciences, University of Michigan, 1000 Wall Street, Ann Arbor, MI 48105; fax: (734) 936-2340; e-mail: [email protected]
1176
AMERICAN JOURNAL
N PIGMENT DISPERSION SYNDROME (PDS) AND EXFOLIA-
OF
OPHTHALMOLOGY
DECEMBER 2003
TABLE 1. Demographics and Clinical Characteristics Age (Years)
Gender
Race
Vision
1
68
F
W
20/300 OU
2 3 4
41 72 46
M F F
W W W
20/15 OU 20/200 OU 20/15 OU
5
33
F
W
20/15 OU
6 7
65 40
F M
W W
20/300 OU 20/15 OU
8
80
F
B
20/25 OU
9
78
M
W
10 11
66 66
F M
W W
20/50 OD 20/100 OS 20/30 OU 20/20 OU
12
67
F
W
13
72
F
W
14
47
M
A
15
81
F
W
Case
20/60 OD 20/200 OS 20/400 OD 20/60 OD 20/200 OD 20/50 OS 20/60 OU
IOP (mm Hg)
Corneal Endopigment*
Mid-peripheral Iris TIDs
Pupillary Ruff
Zonular Free Zone (mm)
TM Pigment†
27 OD 21 OS 10 OU 21 OU 16 OD 17 OS 14 OU
KS OU
Present OD
TIDs OU
ⱕ3.5 OU
4
None OU None OU None OU
Absent OU Absent OU Absent OU
TIDs OU TIDs OU Normal OU
0 3 2
None OU
Absent OU
TIDs OU
KS OU None OU
Absent OU Absent OU
TIDs OU TIDs OU
DP OU
Absent OU
Not reported
KS OU
Absent OU
Normal OU
KS OU None OU
Absent OU Absent OU
Not reported Not reported
2.5 OU ⱕ3.0 OU 3.0 OD 3.1 OS 2.7 OD 3.0 OS ⱕ3.0 OU 3.0 OD 2.7 OS 2.5 OD 2.1 OS IOL OD 4.5 OS Not reported Not reported
None OU
Not reported
Not reported
“Star burst”
2
Not reported
Not reported
Present OU
Not reported
No gonio
Not reported
Not reported
Not reported
Not reported
3–4
None OU
Absent OU
TIDs OU
20 OU 15 OD 13 OS 24 OD 25 OS 13 OD 15 OS 20 OU low 20’s OU 22 OD 19 OS 16 OD 14 OS 30 OD 20 OS 13 OU
3.5 OU
2 3 1, patchy 1, patchy 2–3, patchy 3 2–3, patchy
2
F ⫽ female; M ⫽ male; W ⫽ white; B ⫽ black; A ⫽ Afghan; IOP ⫽ intraocular pressure; OD ⫽ right eye; OS ⫽ left eye; OU ⫽ both eyes; TID ⫽ transillumination defect. *Corneal endopigment was documented either as a Krukenberg spindle (KS), diffuse pattern (DP), or none. † TM ⫽ trabecular meshwork. Pigmentation grading system: 0 ⫽ none, 1 ⫽ faint, 2 ⫽ minimal, 3 ⫽ moderate, 4 ⫽ dense.
FIGURE 1. (A) Long anterior zonules were visible in all cases on the anterior capsule surface, which were apparent on direct illumination and retroillumination after pupillary dilation as in Case 1. (B) Pigment was commonly noted along some of the long anterior zonules as in Case 10.
lin”5 and “retro-iridial lines”6 may represent the same findings. Recently, the prevalence of pigmented lens striae was estimated at 1.8% in a black primary eyecare populaVOL. 136, NO. 6
tion.7 Our electron microscopy results suggest a mechanism of pigment release from the pigmented epithelium located at the pupillary ruff and the central iris, which are
BRIEF REPORTS
1177
FIGURE 2. Transmission electron microscopy of the anterior lens capsule in pigmented long anterior zonules (Case 15). (A) Overview showing a normal central anterior lens capsule, covered by an irregular zonule lamella, and a degenerative lens epithelium (bar is 5 m). (B) Detail of the zonule lamella showing a loose fibrillar substructure and merging with the superficial lens capsule (bar is 1 m). (C) Pigment granules and cell debris are embedded within the thickened zonule lamella (bar is 1 m). (D) Fragments of iris pigment epithelial cells adhere to the irregular zonule lamella (bar is 1 m).
in close proximity to the elongated zonules. The zonules appear normal because standard phacoemulsification did not indicate fragility (Cases 9 and 15). This mechanism is distinct from PDS, in which the iridozonular contact occurs between the midperipheral iris and anterior zonule bundles.8 Though subtle and easily missed on biomicroscopy, the long anterior zonules may be not uncommon but just not previously recognized as a distinct entity associated with pigment dispersion.
2. 3. 4. 5. 6.
ACKNOWLEDGMENTS
The electron micrograph montage was created with the assistance of Mr. Mitch Gillett.
7.
REFERENCES
8.
1. Ayyagari R, Griesinger IB, Bingham E, Lark KK, Moroi SE, Sieving PA. Autosomal dominant hemorrhagic macular dys-
1178
AMERICAN JOURNAL
OF
trophy not associated with the TIMP3 gene. Arch Ophthalmol 2000;118:85–92. Sakabe I, Oshika T, Lim SJ, Apple DJ. Anterior shift of zonular insertion onto the anterior surface of human crystalline lens with age. Ophthalmology 1998;105:295–299. Farnsworth PN, Shyne SE. Anterior zonular shifts with age. Exp Eye Res 1979;28:291–297. Koch DD, Liu JF. Zonular encroachment on the anterior capsular zonular-free zone. Am J Ophthalmol 1988;106:491–92. Abramowicz I. Opacifications strie´ es coronaires superficielles du cristallin. Ann D’Oculistique 1933;170:602–604. Berliner ML. Biomicroscopy of the eye, slit lamp microscopy of the living eye. New York: Paul B. Hoeber, Inc.; 1960: 1023–1024. Roberts DK, Lo PS, Winters JE, Castells DD, Alexander CC, Teitelbaum BA. Prevalence of pigmented lens striae in a black population: a potential indicator of age-related pigment dispersal in the anterior segment. Optom Vis Sci 2002;79:681– 687. Campbell DG. Pigmentary dispersion and glaucoma. A new theory. Arch Ophthalmol 1979;97:1667–1672.
OPHTHALMOLOGY
DECEMBER 2003