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Vitreomacular Observations
Vitreomacular Observations I. Vitreomacular Adhesion and Hole in the Premacular Hyaloid Akihiro Kakehashi, MD, Charles L. Schepens, MD, Clement L. Trempe, MD Purpose: Variations in vitreomacular adhesions and the significance of a hole in the premacular hyaloid membrane were studied clinically to better understand vitreomacular pathology. Methods: With an EI-Bayadi-Kajiura aspheric preset lens, the authors used a vitreous examination technique on 96 eyes, which were divided into three groups. Findings were recorded photographically. Results: Group 1 (25 eyes, 26%) included eyes with a partial posterior vitreous detachment and a residual vitreomacular attachment, but no hole in the premacular hyaloid. All eyes in this group, except one, showed another complication. Diabetic retinopathy and retinal vein occlusion were the most frequent problems noted. Premacular fibrosis, often present in these eyes, may have been precipitated by a vascular complication in the retina. In groups 2 and 3 (71 eyes, 74%), a hole was seen in the premacular hyaloid. Group 2 (46 eyes, 48%) comprised eyes showing a partial posterior vitreous detachment with a strand of vitreous that extruded through the hole in the posterior hyaloid and adhered to the macula. In group 3 (25 eyes, 26%), the hole in the premacular hyaloid was accompanied by a total posterior vitreous detachment. The most common complication noted in eyes in groups 2 and 3 was premacular fibrosis (34 of 71 eyes, 47.9%). The persistence of a residual vitreous attachment to the macula was accompanied by a significantly greater frequency of visual acuity equal to or worse than 20/ 200. Conclusions: Variations in vitreomacular pathology seem to result from differences in the strength of the vitreomacular adhesion and in the process of vitreous liquefaction and shrinkage. In patients with a hole in the premacular hyaloid membrane, the vitreomacular attachment is stronger than the vitreous attachment to other parts of the retina. The latter feature may cause visual acuity deterioration. When there is a hole in the premacular hyaloid membrane, the presence or absence of a vitreomacular adhesion may affect the prognosis for macular function. Ophthalmology 1994;101:1515-1521
To the best of our knowledge, a detailed clinical study of vitreomacular adhesions with or without hole in the premacular hyaloid membrane has not been performed. Our aim is to obtain a better understanding of some forms of vitreomacular pathology and of the significance of holes Originally received: October 2. 1992. Revision accepted: April I, 1994. From the Schepens Eye Research Institute, Harvard Medical School. and Retina Associates, Boston. Reprint requests to Akihiro Kakehashi, MD, Retina Associates, 100 Charles River Plaza, Boston, MA 02114.
in the premacular hyaloid. For this purpose, we reviewed consecutive clinical records of patients with partial posterior vitreous detachment and vitreomacular adhesion and the records of those with premacular hyaloid membrane holes with or without co-existing attachment of extruding vitreous gel to the macula. A persistent vitreomacular adhesion may coexist with several macular diseases, including premacular fibrosis, cystoid macular edema, a vitreomacular traction syndrome, and macular breaks. 1-4 Such adhesion becomes observable after a partial posterior vitreous detachment develops. Even in the absence of any posterior vitreous detachment, vitreo-
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macular traction may cause some forms of vitreomacular pathology such as macular breaks. s-s
Subjects and Methods The 91 patients (96 eyes) studied in this article were examined at the Retina Associates between February 1990 and April 1992. They were consecutive patients with either partial or complete posterior vitreous detachment. To be included in the study, patients with partial posterior vitreous detachment had to present with a vitreomacular adhesion that had formed either with the intact posterior hyaloid membrane or with a strand of vitreous, or with vitreous that extruded through a hole in the premacular hyaloid. Eyes with a complete posterior vitreous detachment were retained for study when they had a hole in the premacular hyaloid membrane. The patients (40 men, 51 women) ranged in age from 26 to 85 years (mean, 64 years). The associated pathology that was found in these eyes is listed in Tables I and 2. Because detection of a vitreomacular attachment through a hole in the hyaloid is difficult, it is best performed with the technique of Takahashi et al 9 using the El Bayadi-Kajiura preset lens (Nikon, Tokyo, Japan) (+58.6 diopter double aspheric). This technique provides strong illumination, a relatively large illumination-observation angle, a large image, and minimal distortion and glare. Because no contact lens is used, the procedure permits dynamic observation of the vitreous during ocular rotation. Because the distance between the macula and a premacular hole in the posterior hyaloid membrane is generally quite short, careful observation is required to detect details. To visualize vitreous gel extruding through a hole in the premacular hyaloid, it is necessary to ask
Diabetic retinopathy* Retinal vein occlusion Idiopathic premacular fibrosis Scleral buckling operation Eales disease Retinal hemangioma Choroidal melanoma Wagner-Stickler syndrome Uveitis Age-related macular degeneration None Total
No. of Eyes 9 4
3 2 1
1 1 1
(%)
(36) (16) (12) (8) (4)
(4) (4) (4) (4) (4)
1
(4)
25
(100)
• All eyes with diabetic retinopathy showed premacular fibrosis with a vascular component.
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Results We classified the vitreomacular pathology observed into three groups.
Table 1. Associated Vitreoretinal Conditions in Group 1 (25 eyes) Associated Condition
the patient to repeat vertical and lateral ocular rotations while using a relatively wide slit beam (0.2 mm). This technique is essential to maximize the Tyndall phenomenon in the vitreous gel. Every effort was made to document findings photographically,9·10 which is often difficult because gel that extrudes through a hole in the hyaloid, or other fine vitreous details, may only be visible for a fleeting moment while the patient's eye is moving. Consequently, many photographic attempts may be necessary to record an important feature. Some observations cannot be recorded in still photographs and require making a movie of the vitreous during rotations of the patient's eye. In particular, a delicate attachment of vitreous gel to the macula often re. . II quires observation of the phenomenon o f jactatwn, which means intermittent traction by a vitreous structure on the retina. One end of the vitreous structure is attached to the retina and the other is attached to the detached vitreous. Traction by the structure on the retina occurs intermittently when the eye rotates and the vitreous gel, which is partly liquefied, moves inside the vitreous cavity. Our findings, therefore, are a combination of photographic recordings with visual observations of the behavior of the vitreous during ocular rotations. Visual observations invariably were made by two or more observers, and patients who could not be photographed adequately were observed with particular attention. All slit-lamp photographs were taken with the slit beam coming from the right and forming a small angle between the axis of observation and the axis of photography (approximately 17°). Therefore, these photographs are not cross-sections, but rather flat views of the retina with the vitreous seen at a slight angle.
Group 1 The 25 (26%) eyes in this group had partial posterior vitreous detachment with vitreomacular adhesion and sometimes adhesion to the disc, but no visible hole in the premacular hyaloid membrane (Fig lA). The vitreomacular adhesion was either with the posterior hyaloid membrane (23 eyes) or with a thin, condensed, vitreous strand that extended from the detached posterior vitreous to the macular area (2 eyes). Eyes in this group represent the classic vitreomacular traction syndrome. Twenty-four of the eyes in this group had another significant fundus condition (Table l ). Diabetic retinopathy was the most frequent complication (9 eyes). Each eye had premacular fibrosis that showed new vessels, distinguishing it from idiopathic premacular fibrosis, which was present in three eyes. Group 2 This group contained 46 eyes (48%) with partial posterior vitreous detachment and vitreomacular adhesion, as in
Kakehashi et al · Vitreomacular Adhesion and Hole in the Premacular Hyaloid Table 2. Associated Vitreoretinal Conditions in Groups 2 and 3 (71 eyes) Associated Condition Premacular fibrosis Idiopathic Secondary Retinal vein occlusion Subclinical or clinical retinal detachment Idiopathic macular break Diabetic retinopathy Age-related macular degeneration Cystoid macular edema (idiopathic) Choroidal melanoma Toxoplasmosis None Total
No. of Eyes
(%)
28 6 10
(39.5) (8.5) (14.1)
6 4 4 3
(8.5) (5.6) (5.6) (4.2)
3 2 1 2
(4.2) (2.8) (1.4) (2.8)
71
(100.0)
group 1, and a hole in the pre macular hyaloid membrane (Fig 1B). All eyes had a premacular hyaloid hole with a strand of vitreous that extruded through that hole and was attached to the macula.
Group 3 Complete posterior vitreous detachment (no vitreomacular adhesion) with a hole in the premacular hyaloid membrane (Fig 1C) was detected in the 25 eyes (26%) in this group. In these eyes, it was assumed that the thin premacular hyaloid that was torn off the vitreous body remained adherent to the macula, together with some prehyaloid vitreous gel. This, however, was never visible on clinical examination. Groups 2 and 3 included a total of 71 eyes (7 4% ). All except two of these eyes had an additional significant ocular condition (Table 2). Premacular fibrosis was the most frequently associated fundus condition. It was found in 34 (47.9%) of the 71 eyes-23 eyes (50%) in group 2 and 11 eyes (44%) in group 3. The difference in percentages is not statistically significant. All eyes with premacular fibrosis reported above excluded those with diabetic retinopathy, because in the eyes with diabetic retinopathy the fibrosis contained new vessels not seen in other eyes with the same condition. Of four eyes with diabetic retinopathy in groups 2 and 3, two showed premacular fibrosis. Table 3 shows the relation between the vitreous condition and visual acuity in eyes with premacular fibrosis in group 2 (vitreomacular adhesion present) and group 3 (total posterior vitreous detachment). Of23 eyes in group 2, 8 (34.8%) showed a best-corrected visual acuity of 20/ 200 or worse. All 11 eyes ( lOO%) in group 3 had a bestcorrected visual acuity greater than 20/200 (P < 0.05, Fisher exact test).
In four instances, the hole in the premacular hyaloid membrane was associated with a macular break. All four macular breaks were observed in group 2, without other retinal disease.
Selected Case Reports Case 1. A 73-year-old woman had idiopathic premacular fibrosis associated with cystoid macular edema in the right eye. Bestcorrected visual acuity was 20/70 in the right eye and 20/30 in the left. Biomicroscopy showed vitreous traction in the area of premacular fibrosis. Asteroid bodies were noted in the vitreous. The condensed posterior hyaloid membrane clearly was traced to the edge of the premacular fibrosis (Fig 2). The partial posterior vitreous detachment demonstrated the existence of an adhesion between the hyaloid membrane and the macula, without a hole in the premacular hyaloid membrane. Case 2. A 46-year-old woman had undergone scleral buckling for retinal detachment in the right eye at 30 years of age and in the left at 29 years of age. Best-corrected visual acuity was 20/ 40 in the right eye and 20/20 in the left. In the left eye, biomicroscopy showed a complete posterior vitreous detachment. The condensed and detached posterior hyaloid membrane could not be traced to the macular area as in case I. Instead, it showed a premacular round defect (Fig 3). No vitreous gel was seen between the hole in the posterior hyaloid and the macula. This patient's eye had a complete posterior vitreous detachment with a hole in the premacular hyaloid membrane and no persistent vitreomacular adhesion. Case 3. A 73-year-old man had a central retinal vein occlusion in the left eye associated with cystoid macular edema. Best-corrected visual acuity was 20/70 in the right eye and hand motion in the left. The vitreous gel in the left eye was slightly turbid due to the central retinal vein occlusion. A partial posterior vitreous detachment with vitreomacular adhesion was present in this eye. The vitreous could not be separated from the macula even with repeated ocular rotations. The detached posterior hyaloid could not be traced to the macular area as in Case 1. The vitreous gel was protruding through a hole in the premacular hyaloid membrane and remained adherent to the macula (Fig 4). Traction on the macula by the vitreous may have aggravated the cystoid macular edema. Case 4. A 67-year-old woman had a small idiopathic macular break in the right eye. Best-corrected visual acuity was 20/200 in the right eye and 20/20 in the left. Biomicroscopy ofthe right eye showed a partial posterior vitreous detachment. The optical section over the disc showed prepapillary glial tissue on the detached posterior hyaloid membrane. In the optical section over the macular area, a hole was seen in the posterior hyaloid membrane. There was no evidence of preretinal membrane around the macular break. The vitreous gel was protruding through the hole in the hyaloid and could not be separated from the macula even with repeated ocular rotations. It remained adherent to the macula through the hole in the premacular hyaloid (Fig 5).
Discussion Three main factors are causing posterior vitreous detachment: loosening of the vitreoretinal adhesion, liquefaction of vitreous gel, and gel shrinkage, all of which occur in age-related posterior vitreous detachment. 12- 18 In diseaserelated posterior vitreous detachment, such as proliferative
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Figure l. Top left, a schematic drawing of virreomac ular adhesion without premacul ar ho le in the poste rio r h yalo id membrane. Top right, a sche· marie drawing of a persistent virreomac ular adhesion through a premacular ho le in the posterio r h ya loid memb rane. Bottom, a schematic drawing of a premacula r hole in the poste rio r hyalo id membrane . o virreomacular adhesion exists, and it is suspected th at to rn premacula r conical vitreous remains adherent ro the macular area.
diabetic retinopathy, shrinkage of the cortical vitreous n often frequently is marked , but the vitreoretinal adhesio 19 23 vitreoA mild. is tion liquefac gel and strong remains macular adhesion may remain, despite gel liquefaction and shrinkage that produces a posterior vitreous detachment elsewhere. This is understandable because the macula normally adheres more25 firmly to the vitreous than 24 other parts of the retina. • This observation probably 26 was first made by Grignolo. in Twenty-three of 25 eyes group 1 showed a residual adhesion of the posterior hyaloid membrane to the mac-
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acular traction synula, representing the classic 4vitreom 27 29 demonstrated in and · ly drome described previous 30 vitreous strand a s, instance two In . histologic sections remained attached to the macula without a visible hole in the premacular hyaloid, which has been observed more rarely. 31 Retinal vascular disease, the most commo n condition associated with group 1 (Table I), was present in 15 eyes (60%) (9 with diabetic retinopathy; 4 with retinal vein occlusion; I with Eales disease; and I with retinal hemangioma). In all these diseases, leakage of blood compo-
Kakehashi et al · Vitreomacular Adhesion and Hole in the Premacular Hyaloid Table 3. Visual Acuity in Eyes with Premacular Fibrosis and no Diabetic Retinopathy Group 1
Group 2
Group 3*
Visual Acuity
No. of Eyes (%)
No. of Eyes (%)
No. of Eyes (%)
>20/200 s20/200
2 (66.7) 1 (33.3)
15 (65.2) 8 (34.8)
11 (100) 0 (0)
Total
3 (100)
23 (100)
11 (100)
• The difference in visual acuity between groups 2 and 3 is significant (P < 0.05).
nents may have induced a condensation of the posterior hyaloid membrane, a reinforcement of the normal vitreomacular adhesion, and vitreous shrinkage with some liquefaction of the gel, leading to subsequent partial posterior vitreous detachment. 32 Diabetic retinopathy typically causes the above-mentioned changes. Inflammation, the second most frequent condition in eyes in group 1, occurred in four eyes ( 16% ): in two after scleral buckling surgery; in one eye associated with malignant choroidal melanoma; and in one eye associated with uveitis. Inflammation also may precipitate partial posterior vitreous detachment and perhaps contribute to reinforcing the vitreomacular adhesion. The type of vitreomacular traction found in eyes in group 1 is well recognized on clinical examination, and severe occurrences may be relieved by vitrectomy. 29 Eyes in groups 2 and 3 had a premacular hyaloid membrane hole, a condition that has been described by several authors. Using biomicroscopy, it was probably first observed in 1955 31 and described by Jaffe. 4 Eisner 33 observed that, in posterior vitreous detachment, a hole often appears in the premacular hyaloid that is larger than that in front of the disc. He indicated that liquid vitreous escapes through that hole into the subhyaloid space and that the hole itself may enlarge considerably as the vitreous body collapses. He also stated that vitreous gel may extrude through that hole. Grignolo, 26 and later Sebag, 24·34 made more detailed but similar observations in dissected human eyes. Observations similar to ours were reported by Kishi and Shimizu (unpublished data; XXIII Meeting of the Club Gonin, Vienna, 1992). This condition should not be confused with a posterior lacuna, in which vitreous gel is replaced by liquid. Such a condition is frequently found in the premacular portion of the vitreous 35- 37 and can easily be distinguished from a hole in the detached premacular hyaloid membrane. The most common complication noted in the eyes in our current study was premacular fibrosis (Table 2). Of 71 eyes, 34 (47.9%) had premacular fibrosis, which was idiopathic in 28 eyes and associated with other retinal diseases in 6. It is possible that premacular fibrosis strengthened the anatomic vitreomacular adhesion, thus preventing detachment of the vitreous from the macula. Because the vitreous cortex is very thin over the macula,
it is easily torn, leaving a premacular round hole in the hyaloid membrane (case 3). One may speculate that a thin layer of premacular vitreous probably remains adherent to the macula in such eyes. If the vitreous cortex had not torn in case 3, the situation would have been analogous to case 1. The patients who showed premacular fibrosis had a visual acuity significantly worse in eyes in group 2 than in those in group 3 (Table 3). Group 2 included eyes with a hole in the premacular hyaloid and a persistent adhesion of the vitreous gel to the macula. Group 3 included similar eyes but without vitreomacular adhesion. The unfavorable effects of a residual adhesion between the hyaloid and the macula has been described previously. 4 Our findings indicate that even the vitreoretinal stress caused by intermittent traction from vitreous gel on the macula may decrease the visual acuity. Retinal vein occlusion was the second most frequent condition in 10 ( 14.1%) of 71 eyes in groups 2 and 3 (Table 2). Leakage ofblood components from retinal vessels may cause acute vitreous gel shrinkage 14 and precipitate the development of a round hole in the premacular hyaloid membrane (case 3). In four eyes, an idiopathic macular break was accompanied by a hole in the premacular hyaloid, through which a vitreous strand extruded and remained attached to the macula (case 4). None of the four eyes showed a hole in the premacular hyaloid without evidence ofvitreomacular adhesion. It is probable that the vitreomacular adhesion and concurrent vitreous traction on the macula caused or at least precipitated the development of the macular break in these eyes. However, it remains possible that the hole in the premacular hyaloid membrane, with residual vitreomacular adhesion, occurred after the development of the macular break. The thinness of the premacular hyaloid membrane, associated with its strong adhesion to the macula, predisposes the hyaloid to tear in this location, even when great care is taken with its dissection. 24•26 •34•38 Sebag24· 34•38 also demonstrated the existence of collagen fibers, within the vitreous, that extend from the macular area toward the vitreous base. In our observations, 48% of the eyes with a premacular hyaloid membrane hole showed that vitreous gel remained adherent to the macula. This indicated that, despite the partial posterior vitreous detachment, the vitreomacular adhesion was sufficiently strong to resist vitreous traction caused by vitreous shrinkage and partial liquefaction. However, the detailed anatomy of the premacular vitreous is still somewhat controversial. 35- 37 · 39.4° Posterior hyaloid membrane that remains adherent to the macula is easy to detect (case 1). In contradistinction, the persistence of a vitreous strand that extrudes through a round hole in the posterior hyaloid and remains adherent to the macula is difficult to diagnose (cases 3 and 4). Because the posterior hyaloid membrane cannot be traced to the site of vitreomacular attachment, a misdiagnosis of complete posterior vitreous detachment easily can be made. Despite this difficulty, persistent vitreous attachment through a hole in the premacular hyaloid was seen in 46 (64.8%) of71 eyes. This was accomplished due to
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0
---A
§:----
Top, Figure 2. Top left, a vitreous photograph of the posterior hyaloid membrane (arrowheads) that is still attached to the premacular fibrosis. Top right, a sketch of the photograph represents vitreomacular adhesion, barely visible optic disc (0), and asteroid bodies (A) in the vitreous.
H
Second row, Figure 3. Second row left, a vitreous photograph of the condensed posterior hyaloid membrane (arrowheads) with a premacular round defect. No vitreous gel is visible between the hole in the posterior hyaloid membrane and macular area. Second row right, a sketch of the photograph represents a posterior hyaloid membrane hole (H), a prepapillary glial remnant (R), and a barely visible optic disc (0). Third row, Figure 4. Third row left, a vitreous photograph of detached turbid vitreous (arrowhead) and a vitreomacular adhesion through a round defect in the posterior hyaloid. Vitreous gel (between arrows) extrudes through a round defect in the posterior hyaloid, is attached to the macula, and cannot be detached from it even with ocular rotations. Third row right, a sketch of the photograph represents extruding vitreous through a round defect in the posterior hyaloid and a vitreomacular attachment. Bottom, Figure 5. Bottom left, a vitreous photograph depicts a vitreomacular attachment in the optical section over the macula. Vitreous gel extrudes (arrows) through a hole in the hyaloid and remains attached above a small macular break, even after ocular rotations. Bottom right, a sketch of the photograph represents vitreous extruding through a defect in the posterior hyaloid, a vitreous attachment above the macular break (MB), and a barely visible optic disc.
0
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Kakehashi et al · Vitreomacular Adhesion and Hole in the Premacular Hyaloid the examination technique used. A correct diagnosis in these eyes is important because it may prevent unnecessary vitrectomy for the treatment of an impending macular break, if it can be established that there is no residual vitreomacular attachment. 6- 8•41 •42
References 1. Gass JDM. Stereoscopic Atlas of Macular Diseases: Diagnosis and Treatment, 3rd ed. Vol. 2. St. Louis: CV Mosby, 1987;671-726. 2. Wise GN. Clinical features of idiopathic preretinal macular fibrosis. Schoenberg Lecture. Am J Ophthalmol 1975;79: 349-57. 3. Schepens CL, Avila MP, Jalkh AE, Trempe CL. Role of the vitreous in cystoid macular edema. Surv Ophthalmol 1984;28:499-504. 4. Jaffe NS. Vitreous traction at the posterior pole of the fundus due to alterations in the vitreous posterior. Trans Am Acad Ophthalmol Otolaryngol 1967;71 :642-52. 5. Avila MP, Jalkh AE, Murakami K, et al. Biomicroscopic study of the vitreous in macular breaks. Ophthalmology 1983;90: 1277-83. 6. Trempe CL, Weiter JJ, Furukawa H. Fellow eyes in cases of macular hole. Biomicroscopic study of the vitreous. Arch Ophthalmol 1986;104:93-5. 7. Gass JDM. Idiopathic senile macular hole: its early stages and pathogenesis. Arch Ophthalmol 1988;106:629-39. 8. Akiba J, Quiroz MA, Trempe CL. Role of posterior vitreous detachment in idiopathic macular holes. Ophthalmology 1990;97: 1610-13. 9. Takahashi M, Trempe CL, Schepens CL. Biomicroscopic evaluation and photography of posterior vitreous detachment. Arch Ophthalmol 1980;98:665-8. 10. Kakehashi A, Akiba J, Trempe CL. Vitreous photography with a +90-diopter double aspheric preset lens vs the El Bayadi-Kajiura preset lens. Arch Ophthalmol 1991;109: 962-5. 11. Vogt A, Lehrbuch und Atlas des Spaltlampenmikroskopie des lebendes Auges. Vol. 3. Stuttgart: Enke, 1942;972-5. 12. Goldmann H. Senescenz des Glaskorpers. Ophthalmologica 1962;143:253-79. 13. Eisner G. Zur Anatomie des Glaskorpers. Albrecht Von Graefes Arch Klin Exp Ophthalmol 1975;193:33-56. 14. O'Malley P. The pattern of vitreous syneresis. A study of 800 autopsy eyes. In: Irvine AR, O'Malley C, eds. Advances in Vitreous Surgery. Springfield: Charles C Thomas, 1976; chap. 2. 15. Tolentino Fl, Schepens CL, Freeman HM. Vitreoretinal Disorders: Diagnosis and Management. Philadelphia: WB Saunders, 1976;130-50. 16. Balazs EA, Denlinger JL. Aging changes in the vitreous. In: Sekular R, Kline D, Dismukes K, eds. Aging and Human Visual Function. New York: Alan R Liss, 1982;45-57. (Mod Aging Res; 2). 17. Foos RY, Wheeler NC. Vitreoretinal juncture. Synchysis senilis and posterior vitreous detachment. Ophthalmology 1982;89: 1502-12. 18. Larsson L, Osterlin S. Posterior vitreous detachment. A combined clinical and physiochemical study. Graefes Arch Clin Exp Ophthalmol 1985;223:92-5.
19. Davis MD. Vitreous contraction in proliferative diabetic retinopathy. Arch Ophthalmol 1965;74:741-51. 20. Tolentino FI, Lee P-F, Schepens CL. Biomicroscopic study of vitreous cavity in diabetic retinopathy. Arch Ophthalmol 1966;75:238-46. 21. Takahashi M, Trempe CL, Maguire K, McMeel JW. Vitreoretinal relationship in diabetic retinopathy. A biomicroscopic evaluation. Arch Ophthalmol 1981 ;99:241-5. 22. Jalkh A, Takahashi M, Topilow HW, et al. Prognostic value of vitreous findings in diabetic retinopathy. Arch Ophthalmol 1982; 100:432-4. 23. Akiba J, Arzabe CW, Trempe CL. Posterior vitreous detachment and neovascularization in diabetic retinopathy. Ophthalmology 1990;97:889-91. 24. Sebag J. Age-related difference in the human vitreoretinal interface. Arch Ophthalmol 1991; 109:966-71. 25. Schachat AP, Sommer A. Macular hemorrhages associated with posterior vitreous detachment. Am J Ophthalmol 1986;102:647-9. 26. Grignolo A. Fibrous components of the vitreous body. Arch Ophthalmol1952;47:760-74. 27. Tolentino FI, Schepens CL. Edema of posterior pole after cataract extraction. A biomicroscopic study. Arch Ophthalmol 1965;74:781-6. 28. Michels RG. Vitreous Surgery. St. Louis: CV Mosby, 1981;11, 354. 29. Smiddy WE, Michels RG, Glaser BM, deBustros S. Vitrectomy for macular traction caused by incomplete vitreous separation. Arch Ophthalmol 1988;106:624-8. 30. Reese AB, Jones IS, Cooper WC. Vitreomacular traction syndrome confirmed histologically. Am J Ophthalmol 1970;69:97 5-7. 31. Schepens CL. Fundus changes caused by alterations of the vitreous body. Am J Ophthalmol 1955;39:631-3. 32. Akiba J, Kado M, Kakehashi A, Trempe CL. Role of the vitreous in posterior segment neovascularization in central retinal vein occlusion. Ophthalmic Surg 1991 ;22:498-502. 33. Eisner G. The anatomy and biomicroscopy of the vitreous body. In: Deutman AF, ed. New Developments in Ophthalmology. The Hague: Dr. W. Junk, 1976:87-104 (Doc Ophthalmol Proc Ser;7). 34. Sebag J. The Vitreous: Structure, Function, and Pathobiology. New York: Springer-Verlag; 40-58. 35. Worst JGF. The bursa intravitrealis premacularis. In: Deutman AF, ed. New Developments in Ophthalmology. The Hague: Dr. W. Junk, 1976;275-9 (Doc Ophthalmol Proc Ser;7). 36. Kishi S, Shimizu K. Posterior precortical vitreous pocket. Arch Ophthalmol 1990;108:979-82. 37. Worst JGF. Posterior precortical vitreous pocket [letter]. Arch Ophthalmol 1991; 109: 1058-9. 38. Sebag J. Age-related changes in human vitreous structure. Graefes Arch Clin Exp Ophthalmol 1987;225:89-93. 39. Worst JGF. Cisternal systems of the fully developed vitreous body in the young adult. Trans Ophthalmol Soc UK 1977;97:550-4. 40. Kishi S, Shimizu K. Reply, 1060. To: Worst JGF and Sebag J. Posterior precortical vitreous pocket [letters]. Arch Ophthalmol 1991; 109: 1058-60. 41. Akiba J, Yoshida A, Trempe CL. Risk of developing a macular hole. Arch Ophthalmol 1990;108:1088-90. 42. Wiznia RA. Reversibility of the early stages of idiopathic macular holes. Am J Ophthalmol 1989;107:241-5.
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To the best of our knowledge, a detailed clinical study of vitreomacular adhesions with or without hole in the premacular hyaloid membrane has not been performed. Our aim is to obtain a better understanding of some forms of vitreomacular pathology and of the significance of holes Originally received: October 2. 1992. Revision accepted: April I, 1994. From the Schepens Eye Research Institute, Harvard Medical School. and Retina Associates, Boston. Reprint requests to Akihiro Kakehashi, MD, Retina Associates, 100 Charles River Plaza, Boston, MA 02114.
in the premacular hyaloid. For this purpose, we reviewed consecutive clinical records of patients with partial posterior vitreous detachment and vitreomacular adhesion and the records of those with premacular hyaloid membrane holes with or without co-existing attachment of extruding vitreous gel to the macula. A persistent vitreomacular adhesion may coexist with several macular diseases, including premacular fibrosis, cystoid macular edema, a vitreomacular traction syndrome, and macular breaks. 1-4 Such adhesion becomes observable after a partial posterior vitreous detachment develops. Even in the absence of any posterior vitreous detachment, vitreo-
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macular traction may cause some forms of vitreomacular pathology such as macular breaks. s-s
Subjects and Methods The 91 patients (96 eyes) studied in this article were examined at the Retina Associates between February 1990 and April 1992. They were consecutive patients with either partial or complete posterior vitreous detachment. To be included in the study, patients with partial posterior vitreous detachment had to present with a vitreomacular adhesion that had formed either with the intact posterior hyaloid membrane or with a strand of vitreous, or with vitreous that extruded through a hole in the premacular hyaloid. Eyes with a complete posterior vitreous detachment were retained for study when they had a hole in the premacular hyaloid membrane. The patients (40 men, 51 women) ranged in age from 26 to 85 years (mean, 64 years). The associated pathology that was found in these eyes is listed in Tables I and 2. Because detection of a vitreomacular attachment through a hole in the hyaloid is difficult, it is best performed with the technique of Takahashi et al 9 using the El Bayadi-Kajiura preset lens (Nikon, Tokyo, Japan) (+58.6 diopter double aspheric). This technique provides strong illumination, a relatively large illumination-observation angle, a large image, and minimal distortion and glare. Because no contact lens is used, the procedure permits dynamic observation of the vitreous during ocular rotation. Because the distance between the macula and a premacular hole in the posterior hyaloid membrane is generally quite short, careful observation is required to detect details. To visualize vitreous gel extruding through a hole in the premacular hyaloid, it is necessary to ask
Diabetic retinopathy* Retinal vein occlusion Idiopathic premacular fibrosis Scleral buckling operation Eales disease Retinal hemangioma Choroidal melanoma Wagner-Stickler syndrome Uveitis Age-related macular degeneration None Total
No. of Eyes 9 4
3 2 1
1 1 1
(%)
(36) (16) (12) (8) (4)
(4) (4) (4) (4) (4)
1
(4)
25
(100)
• All eyes with diabetic retinopathy showed premacular fibrosis with a vascular component.
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Results We classified the vitreomacular pathology observed into three groups.
Table 1. Associated Vitreoretinal Conditions in Group 1 (25 eyes) Associated Condition
the patient to repeat vertical and lateral ocular rotations while using a relatively wide slit beam (0.2 mm). This technique is essential to maximize the Tyndall phenomenon in the vitreous gel. Every effort was made to document findings photographically,9·10 which is often difficult because gel that extrudes through a hole in the hyaloid, or other fine vitreous details, may only be visible for a fleeting moment while the patient's eye is moving. Consequently, many photographic attempts may be necessary to record an important feature. Some observations cannot be recorded in still photographs and require making a movie of the vitreous during rotations of the patient's eye. In particular, a delicate attachment of vitreous gel to the macula often re. . II quires observation of the phenomenon o f jactatwn, which means intermittent traction by a vitreous structure on the retina. One end of the vitreous structure is attached to the retina and the other is attached to the detached vitreous. Traction by the structure on the retina occurs intermittently when the eye rotates and the vitreous gel, which is partly liquefied, moves inside the vitreous cavity. Our findings, therefore, are a combination of photographic recordings with visual observations of the behavior of the vitreous during ocular rotations. Visual observations invariably were made by two or more observers, and patients who could not be photographed adequately were observed with particular attention. All slit-lamp photographs were taken with the slit beam coming from the right and forming a small angle between the axis of observation and the axis of photography (approximately 17°). Therefore, these photographs are not cross-sections, but rather flat views of the retina with the vitreous seen at a slight angle.
Group 1 The 25 (26%) eyes in this group had partial posterior vitreous detachment with vitreomacular adhesion and sometimes adhesion to the disc, but no visible hole in the premacular hyaloid membrane (Fig lA). The vitreomacular adhesion was either with the posterior hyaloid membrane (23 eyes) or with a thin, condensed, vitreous strand that extended from the detached posterior vitreous to the macular area (2 eyes). Eyes in this group represent the classic vitreomacular traction syndrome. Twenty-four of the eyes in this group had another significant fundus condition (Table l ). Diabetic retinopathy was the most frequent complication (9 eyes). Each eye had premacular fibrosis that showed new vessels, distinguishing it from idiopathic premacular fibrosis, which was present in three eyes. Group 2 This group contained 46 eyes (48%) with partial posterior vitreous detachment and vitreomacular adhesion, as in
Kakehashi et al · Vitreomacular Adhesion and Hole in the Premacular Hyaloid Table 2. Associated Vitreoretinal Conditions in Groups 2 and 3 (71 eyes) Associated Condition Premacular fibrosis Idiopathic Secondary Retinal vein occlusion Subclinical or clinical retinal detachment Idiopathic macular break Diabetic retinopathy Age-related macular degeneration Cystoid macular edema (idiopathic) Choroidal melanoma Toxoplasmosis None Total
No. of Eyes
(%)
28 6 10
(39.5) (8.5) (14.1)
6 4 4 3
(8.5) (5.6) (5.6) (4.2)
3 2 1 2
(4.2) (2.8) (1.4) (2.8)
71
(100.0)
group 1, and a hole in the pre macular hyaloid membrane (Fig 1B). All eyes had a premacular hyaloid hole with a strand of vitreous that extruded through that hole and was attached to the macula.
Group 3 Complete posterior vitreous detachment (no vitreomacular adhesion) with a hole in the premacular hyaloid membrane (Fig 1C) was detected in the 25 eyes (26%) in this group. In these eyes, it was assumed that the thin premacular hyaloid that was torn off the vitreous body remained adherent to the macula, together with some prehyaloid vitreous gel. This, however, was never visible on clinical examination. Groups 2 and 3 included a total of 71 eyes (7 4% ). All except two of these eyes had an additional significant ocular condition (Table 2). Premacular fibrosis was the most frequently associated fundus condition. It was found in 34 (47.9%) of the 71 eyes-23 eyes (50%) in group 2 and 11 eyes (44%) in group 3. The difference in percentages is not statistically significant. All eyes with premacular fibrosis reported above excluded those with diabetic retinopathy, because in the eyes with diabetic retinopathy the fibrosis contained new vessels not seen in other eyes with the same condition. Of four eyes with diabetic retinopathy in groups 2 and 3, two showed premacular fibrosis. Table 3 shows the relation between the vitreous condition and visual acuity in eyes with premacular fibrosis in group 2 (vitreomacular adhesion present) and group 3 (total posterior vitreous detachment). Of23 eyes in group 2, 8 (34.8%) showed a best-corrected visual acuity of 20/ 200 or worse. All 11 eyes ( lOO%) in group 3 had a bestcorrected visual acuity greater than 20/200 (P < 0.05, Fisher exact test).
In four instances, the hole in the premacular hyaloid membrane was associated with a macular break. All four macular breaks were observed in group 2, without other retinal disease.
Selected Case Reports Case 1. A 73-year-old woman had idiopathic premacular fibrosis associated with cystoid macular edema in the right eye. Bestcorrected visual acuity was 20/70 in the right eye and 20/30 in the left. Biomicroscopy showed vitreous traction in the area of premacular fibrosis. Asteroid bodies were noted in the vitreous. The condensed posterior hyaloid membrane clearly was traced to the edge of the premacular fibrosis (Fig 2). The partial posterior vitreous detachment demonstrated the existence of an adhesion between the hyaloid membrane and the macula, without a hole in the premacular hyaloid membrane. Case 2. A 46-year-old woman had undergone scleral buckling for retinal detachment in the right eye at 30 years of age and in the left at 29 years of age. Best-corrected visual acuity was 20/ 40 in the right eye and 20/20 in the left. In the left eye, biomicroscopy showed a complete posterior vitreous detachment. The condensed and detached posterior hyaloid membrane could not be traced to the macular area as in case I. Instead, it showed a premacular round defect (Fig 3). No vitreous gel was seen between the hole in the posterior hyaloid and the macula. This patient's eye had a complete posterior vitreous detachment with a hole in the premacular hyaloid membrane and no persistent vitreomacular adhesion. Case 3. A 73-year-old man had a central retinal vein occlusion in the left eye associated with cystoid macular edema. Best-corrected visual acuity was 20/70 in the right eye and hand motion in the left. The vitreous gel in the left eye was slightly turbid due to the central retinal vein occlusion. A partial posterior vitreous detachment with vitreomacular adhesion was present in this eye. The vitreous could not be separated from the macula even with repeated ocular rotations. The detached posterior hyaloid could not be traced to the macular area as in Case 1. The vitreous gel was protruding through a hole in the premacular hyaloid membrane and remained adherent to the macula (Fig 4). Traction on the macula by the vitreous may have aggravated the cystoid macular edema. Case 4. A 67-year-old woman had a small idiopathic macular break in the right eye. Best-corrected visual acuity was 20/200 in the right eye and 20/20 in the left. Biomicroscopy ofthe right eye showed a partial posterior vitreous detachment. The optical section over the disc showed prepapillary glial tissue on the detached posterior hyaloid membrane. In the optical section over the macular area, a hole was seen in the posterior hyaloid membrane. There was no evidence of preretinal membrane around the macular break. The vitreous gel was protruding through the hole in the hyaloid and could not be separated from the macula even with repeated ocular rotations. It remained adherent to the macula through the hole in the premacular hyaloid (Fig 5).
Discussion Three main factors are causing posterior vitreous detachment: loosening of the vitreoretinal adhesion, liquefaction of vitreous gel, and gel shrinkage, all of which occur in age-related posterior vitreous detachment. 12- 18 In diseaserelated posterior vitreous detachment, such as proliferative
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Volume 101, Numbe r 9, September 1994
Figure l. Top left, a schematic drawing of virreomac ular adhesion without premacul ar ho le in the poste rio r h yalo id membrane. Top right, a sche· marie drawing of a persistent virreomac ular adhesion through a premacular ho le in the posterio r h ya loid memb rane. Bottom, a schematic drawing of a premacula r hole in the poste rio r hyalo id membrane . o virreomacular adhesion exists, and it is suspected th at to rn premacula r conical vitreous remains adherent ro the macular area.
diabetic retinopathy, shrinkage of the cortical vitreous n often frequently is marked , but the vitreoretinal adhesio 19 23 vitreoA mild. is tion liquefac gel and strong remains macular adhesion may remain, despite gel liquefaction and shrinkage that produces a posterior vitreous detachment elsewhere. This is understandable because the macula normally adheres more25 firmly to the vitreous than 24 other parts of the retina. • This observation probably 26 was first made by Grignolo. in Twenty-three of 25 eyes group 1 showed a residual adhesion of the posterior hyaloid membrane to the mac-
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acular traction synula, representing the classic 4vitreom 27 29 demonstrated in and · ly drome described previous 30 vitreous strand a s, instance two In . histologic sections remained attached to the macula without a visible hole in the premacular hyaloid, which has been observed more rarely. 31 Retinal vascular disease, the most commo n condition associated with group 1 (Table I), was present in 15 eyes (60%) (9 with diabetic retinopathy; 4 with retinal vein occlusion; I with Eales disease; and I with retinal hemangioma). In all these diseases, leakage of blood compo-
Kakehashi et al · Vitreomacular Adhesion and Hole in the Premacular Hyaloid Table 3. Visual Acuity in Eyes with Premacular Fibrosis and no Diabetic Retinopathy Group 1
Group 2
Group 3*
Visual Acuity
No. of Eyes (%)
No. of Eyes (%)
No. of Eyes (%)
>20/200 s20/200
2 (66.7) 1 (33.3)
15 (65.2) 8 (34.8)
11 (100) 0 (0)
Total
3 (100)
23 (100)
11 (100)
• The difference in visual acuity between groups 2 and 3 is significant (P < 0.05).
nents may have induced a condensation of the posterior hyaloid membrane, a reinforcement of the normal vitreomacular adhesion, and vitreous shrinkage with some liquefaction of the gel, leading to subsequent partial posterior vitreous detachment. 32 Diabetic retinopathy typically causes the above-mentioned changes. Inflammation, the second most frequent condition in eyes in group 1, occurred in four eyes ( 16% ): in two after scleral buckling surgery; in one eye associated with malignant choroidal melanoma; and in one eye associated with uveitis. Inflammation also may precipitate partial posterior vitreous detachment and perhaps contribute to reinforcing the vitreomacular adhesion. The type of vitreomacular traction found in eyes in group 1 is well recognized on clinical examination, and severe occurrences may be relieved by vitrectomy. 29 Eyes in groups 2 and 3 had a premacular hyaloid membrane hole, a condition that has been described by several authors. Using biomicroscopy, it was probably first observed in 1955 31 and described by Jaffe. 4 Eisner 33 observed that, in posterior vitreous detachment, a hole often appears in the premacular hyaloid that is larger than that in front of the disc. He indicated that liquid vitreous escapes through that hole into the subhyaloid space and that the hole itself may enlarge considerably as the vitreous body collapses. He also stated that vitreous gel may extrude through that hole. Grignolo, 26 and later Sebag, 24·34 made more detailed but similar observations in dissected human eyes. Observations similar to ours were reported by Kishi and Shimizu (unpublished data; XXIII Meeting of the Club Gonin, Vienna, 1992). This condition should not be confused with a posterior lacuna, in which vitreous gel is replaced by liquid. Such a condition is frequently found in the premacular portion of the vitreous 35- 37 and can easily be distinguished from a hole in the detached premacular hyaloid membrane. The most common complication noted in the eyes in our current study was premacular fibrosis (Table 2). Of 71 eyes, 34 (47.9%) had premacular fibrosis, which was idiopathic in 28 eyes and associated with other retinal diseases in 6. It is possible that premacular fibrosis strengthened the anatomic vitreomacular adhesion, thus preventing detachment of the vitreous from the macula. Because the vitreous cortex is very thin over the macula,
it is easily torn, leaving a premacular round hole in the hyaloid membrane (case 3). One may speculate that a thin layer of premacular vitreous probably remains adherent to the macula in such eyes. If the vitreous cortex had not torn in case 3, the situation would have been analogous to case 1. The patients who showed premacular fibrosis had a visual acuity significantly worse in eyes in group 2 than in those in group 3 (Table 3). Group 2 included eyes with a hole in the premacular hyaloid and a persistent adhesion of the vitreous gel to the macula. Group 3 included similar eyes but without vitreomacular adhesion. The unfavorable effects of a residual adhesion between the hyaloid and the macula has been described previously. 4 Our findings indicate that even the vitreoretinal stress caused by intermittent traction from vitreous gel on the macula may decrease the visual acuity. Retinal vein occlusion was the second most frequent condition in 10 ( 14.1%) of 71 eyes in groups 2 and 3 (Table 2). Leakage ofblood components from retinal vessels may cause acute vitreous gel shrinkage 14 and precipitate the development of a round hole in the premacular hyaloid membrane (case 3). In four eyes, an idiopathic macular break was accompanied by a hole in the premacular hyaloid, through which a vitreous strand extruded and remained attached to the macula (case 4). None of the four eyes showed a hole in the premacular hyaloid without evidence ofvitreomacular adhesion. It is probable that the vitreomacular adhesion and concurrent vitreous traction on the macula caused or at least precipitated the development of the macular break in these eyes. However, it remains possible that the hole in the premacular hyaloid membrane, with residual vitreomacular adhesion, occurred after the development of the macular break. The thinness of the premacular hyaloid membrane, associated with its strong adhesion to the macula, predisposes the hyaloid to tear in this location, even when great care is taken with its dissection. 24•26 •34•38 Sebag24· 34•38 also demonstrated the existence of collagen fibers, within the vitreous, that extend from the macular area toward the vitreous base. In our observations, 48% of the eyes with a premacular hyaloid membrane hole showed that vitreous gel remained adherent to the macula. This indicated that, despite the partial posterior vitreous detachment, the vitreomacular adhesion was sufficiently strong to resist vitreous traction caused by vitreous shrinkage and partial liquefaction. However, the detailed anatomy of the premacular vitreous is still somewhat controversial. 35- 37 · 39.4° Posterior hyaloid membrane that remains adherent to the macula is easy to detect (case 1). In contradistinction, the persistence of a vitreous strand that extrudes through a round hole in the posterior hyaloid and remains adherent to the macula is difficult to diagnose (cases 3 and 4). Because the posterior hyaloid membrane cannot be traced to the site of vitreomacular attachment, a misdiagnosis of complete posterior vitreous detachment easily can be made. Despite this difficulty, persistent vitreous attachment through a hole in the premacular hyaloid was seen in 46 (64.8%) of71 eyes. This was accomplished due to
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0
---A
§:----
Top, Figure 2. Top left, a vitreous photograph of the posterior hyaloid membrane (arrowheads) that is still attached to the premacular fibrosis. Top right, a sketch of the photograph represents vitreomacular adhesion, barely visible optic disc (0), and asteroid bodies (A) in the vitreous.
H
Second row, Figure 3. Second row left, a vitreous photograph of the condensed posterior hyaloid membrane (arrowheads) with a premacular round defect. No vitreous gel is visible between the hole in the posterior hyaloid membrane and macular area. Second row right, a sketch of the photograph represents a posterior hyaloid membrane hole (H), a prepapillary glial remnant (R), and a barely visible optic disc (0). Third row, Figure 4. Third row left, a vitreous photograph of detached turbid vitreous (arrowhead) and a vitreomacular adhesion through a round defect in the posterior hyaloid. Vitreous gel (between arrows) extrudes through a round defect in the posterior hyaloid, is attached to the macula, and cannot be detached from it even with ocular rotations. Third row right, a sketch of the photograph represents extruding vitreous through a round defect in the posterior hyaloid and a vitreomacular attachment. Bottom, Figure 5. Bottom left, a vitreous photograph depicts a vitreomacular attachment in the optical section over the macula. Vitreous gel extrudes (arrows) through a hole in the hyaloid and remains attached above a small macular break, even after ocular rotations. Bottom right, a sketch of the photograph represents vitreous extruding through a defect in the posterior hyaloid, a vitreous attachment above the macular break (MB), and a barely visible optic disc.
0
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Kakehashi et al · Vitreomacular Adhesion and Hole in the Premacular Hyaloid the examination technique used. A correct diagnosis in these eyes is important because it may prevent unnecessary vitrectomy for the treatment of an impending macular break, if it can be established that there is no residual vitreomacular attachment. 6- 8•41 •42
References 1. Gass JDM. Stereoscopic Atlas of Macular Diseases: Diagnosis and Treatment, 3rd ed. Vol. 2. St. Louis: CV Mosby, 1987;671-726. 2. Wise GN. Clinical features of idiopathic preretinal macular fibrosis. Schoenberg Lecture. Am J Ophthalmol 1975;79: 349-57. 3. Schepens CL, Avila MP, Jalkh AE, Trempe CL. Role of the vitreous in cystoid macular edema. Surv Ophthalmol 1984;28:499-504. 4. Jaffe NS. Vitreous traction at the posterior pole of the fundus due to alterations in the vitreous posterior. Trans Am Acad Ophthalmol Otolaryngol 1967;71 :642-52. 5. Avila MP, Jalkh AE, Murakami K, et al. Biomicroscopic study of the vitreous in macular breaks. Ophthalmology 1983;90: 1277-83. 6. Trempe CL, Weiter JJ, Furukawa H. Fellow eyes in cases of macular hole. Biomicroscopic study of the vitreous. Arch Ophthalmol 1986;104:93-5. 7. Gass JDM. Idiopathic senile macular hole: its early stages and pathogenesis. Arch Ophthalmol 1988;106:629-39. 8. Akiba J, Quiroz MA, Trempe CL. Role of posterior vitreous detachment in idiopathic macular holes. Ophthalmology 1990;97: 1610-13. 9. Takahashi M, Trempe CL, Schepens CL. Biomicroscopic evaluation and photography of posterior vitreous detachment. Arch Ophthalmol 1980;98:665-8. 10. Kakehashi A, Akiba J, Trempe CL. Vitreous photography with a +90-diopter double aspheric preset lens vs the El Bayadi-Kajiura preset lens. Arch Ophthalmol 1991;109: 962-5. 11. Vogt A, Lehrbuch und Atlas des Spaltlampenmikroskopie des lebendes Auges. Vol. 3. Stuttgart: Enke, 1942;972-5. 12. Goldmann H. Senescenz des Glaskorpers. Ophthalmologica 1962;143:253-79. 13. Eisner G. Zur Anatomie des Glaskorpers. Albrecht Von Graefes Arch Klin Exp Ophthalmol 1975;193:33-56. 14. O'Malley P. The pattern of vitreous syneresis. A study of 800 autopsy eyes. In: Irvine AR, O'Malley C, eds. Advances in Vitreous Surgery. Springfield: Charles C Thomas, 1976; chap. 2. 15. Tolentino Fl, Schepens CL, Freeman HM. Vitreoretinal Disorders: Diagnosis and Management. Philadelphia: WB Saunders, 1976;130-50. 16. Balazs EA, Denlinger JL. Aging changes in the vitreous. In: Sekular R, Kline D, Dismukes K, eds. Aging and Human Visual Function. New York: Alan R Liss, 1982;45-57. (Mod Aging Res; 2). 17. Foos RY, Wheeler NC. Vitreoretinal juncture. Synchysis senilis and posterior vitreous detachment. Ophthalmology 1982;89: 1502-12. 18. Larsson L, Osterlin S. Posterior vitreous detachment. A combined clinical and physiochemical study. Graefes Arch Clin Exp Ophthalmol 1985;223:92-5.
19. Davis MD. Vitreous contraction in proliferative diabetic retinopathy. Arch Ophthalmol 1965;74:741-51. 20. Tolentino FI, Lee P-F, Schepens CL. Biomicroscopic study of vitreous cavity in diabetic retinopathy. Arch Ophthalmol 1966;75:238-46. 21. Takahashi M, Trempe CL, Maguire K, McMeel JW. Vitreoretinal relationship in diabetic retinopathy. A biomicroscopic evaluation. Arch Ophthalmol 1981 ;99:241-5. 22. Jalkh A, Takahashi M, Topilow HW, et al. Prognostic value of vitreous findings in diabetic retinopathy. Arch Ophthalmol 1982; 100:432-4. 23. Akiba J, Arzabe CW, Trempe CL. Posterior vitreous detachment and neovascularization in diabetic retinopathy. Ophthalmology 1990;97:889-91. 24. Sebag J. Age-related difference in the human vitreoretinal interface. Arch Ophthalmol 1991; 109:966-71. 25. Schachat AP, Sommer A. Macular hemorrhages associated with posterior vitreous detachment. Am J Ophthalmol 1986;102:647-9. 26. Grignolo A. Fibrous components of the vitreous body. Arch Ophthalmol1952;47:760-74. 27. Tolentino FI, Schepens CL. Edema of posterior pole after cataract extraction. A biomicroscopic study. Arch Ophthalmol 1965;74:781-6. 28. Michels RG. Vitreous Surgery. St. Louis: CV Mosby, 1981;11, 354. 29. Smiddy WE, Michels RG, Glaser BM, deBustros S. Vitrectomy for macular traction caused by incomplete vitreous separation. Arch Ophthalmol 1988;106:624-8. 30. Reese AB, Jones IS, Cooper WC. Vitreomacular traction syndrome confirmed histologically. Am J Ophthalmol 1970;69:97 5-7. 31. Schepens CL. Fundus changes caused by alterations of the vitreous body. Am J Ophthalmol 1955;39:631-3. 32. Akiba J, Kado M, Kakehashi A, Trempe CL. Role of the vitreous in posterior segment neovascularization in central retinal vein occlusion. Ophthalmic Surg 1991 ;22:498-502. 33. Eisner G. The anatomy and biomicroscopy of the vitreous body. In: Deutman AF, ed. New Developments in Ophthalmology. The Hague: Dr. W. Junk, 1976:87-104 (Doc Ophthalmol Proc Ser;7). 34. Sebag J. The Vitreous: Structure, Function, and Pathobiology. New York: Springer-Verlag; 40-58. 35. Worst JGF. The bursa intravitrealis premacularis. In: Deutman AF, ed. New Developments in Ophthalmology. The Hague: Dr. W. Junk, 1976;275-9 (Doc Ophthalmol Proc Ser;7). 36. Kishi S, Shimizu K. Posterior precortical vitreous pocket. Arch Ophthalmol 1990;108:979-82. 37. Worst JGF. Posterior precortical vitreous pocket [letter]. Arch Ophthalmol 1991; 109: 1058-9. 38. Sebag J. Age-related changes in human vitreous structure. Graefes Arch Clin Exp Ophthalmol 1987;225:89-93. 39. Worst JGF. Cisternal systems of the fully developed vitreous body in the young adult. Trans Ophthalmol Soc UK 1977;97:550-4. 40. Kishi S, Shimizu K. Reply, 1060. To: Worst JGF and Sebag J. Posterior precortical vitreous pocket [letters]. Arch Ophthalmol 1991; 109: 1058-60. 41. Akiba J, Yoshida A, Trempe CL. Risk of developing a macular hole. Arch Ophthalmol 1990;108:1088-90. 42. Wiznia RA. Reversibility of the early stages of idiopathic macular holes. Am J Ophthalmol 1989;107:241-5.
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