Epiretinal pathology of diffuse diabetic macular edema associated with vitreomacular traction

doi:10.1016/j.ajo.2004.11.035

American Journal of Ophthalmology

Volume 139, Issue 4, April 2005, Pages 638-652

https://doi.org/10.1016/j.ajo.2004.11.035 Get rights and content

Purpose

To investigate the ultrastructure of the vitreomacular interface in patients with diffuse diabetic macular edema (DDME) associated with vitreomacular traction.

Design

Laboratory investigation.

Methods

Fifty-five consecutive patients with DDME underwent vitrectomy with en-bloc removal of the inner limiting membrane (ILM) and epimacular tissue. Six patients were operated on both eyes. Sixty-one specimens harvested during vitrectomy were analyzed by electron microscopy.

Results

Preoperatively, a thickened premacular cortical vitreous was present in 47 eyes. Native vitreous collagen with single cells interspersed within the collagenous layer or a cellular monolayer were the ultrastructural features in these eyes. Twenty-three eyes showed an epimacular membrane. In eyes with obvious signs of tangential vitreomacular traction, multilayered membranes situated on a layer of native vitreous collagen were found. Fibroblasts and fibrous astrocytes were the predominant cell types; myofibroblasts and macrophages were also present. Sixty of 61 specimens showed native vitreous collagen covering the ILM. Macular edema resolved in 58 eyes and persisted in 3 eyes. No recurrent fibrocellular proliferation was observed during the follow-up period of 18 months (mean, 3 to 56 months).

Conclusions

The vitreomacular interface in eyes with DDME is characterized by a layer of native vitreous collagen and a varying cellular component. Tangential vitreomacular traction is associated with multilayered membranes situated on a layer of vitreous collagen. Resolution of macular edema does not depend on the presence and removal of contractile membranes. In eyes without tangential traction, complete removal of epimacular tissue also leads to fluid resorption.

Section snippets

Methods

Between April 1997 and April 2003, 77 patients underwent en-bloc dissection of the ILM and epimacular tissue attributable to DDME. In 55 patients the retinal specimens were harvested and successfully processed for electron microscopy. These patients are included in this retrospective study. Approval from the Institutional Review Board and informed consent were obtained.

Indication for surgery was based on the three following criteria: (1) diagnosis of DDME, confirmed by fluorescein angiography,

Preoperative data

The clinical characteristics of 61 eyes of 55 patients included in the study are summarized in Table 2. Fourteen patients were female and 41 were male. Ages ranged from 25 to 80 years, with a mean age of 60 years. A total of 54 eyes had proliferative diabetic retinopathy (PDR) and 7 eyes had non-proliferative diabetic retinopathy (NPDR). Eight patients had type I diabetes and 47 patients had type II diabetes. Forty-nine eyes were phakic at the time of vitrectomy and, 12 eyes had a posterior

Discussion

In 1993, Kishi and Shimizu reported the clinical manifestations of the premacular vitreous in PDR.²⁵ In 94% of their 134 study eyes with partial PVD, a posterior precortical vitreous pocket was observed in front of the macula.²⁵ The posterior border of this pocket was formed by the premacular cortical vitreous, which remained attached to the macula.²⁵ Schwartz and associates identified cortical vitreous remaining attached to the macula (so-called vitreoschisis) during surgery in 145 (81%) of

PD Dr. Arnd Gandorfer is a vitreoretinal surgeon at the University Eye Hospital Munich, Germany, and head of the electron microscopy unit (Eye Morphology Center, Munich). Most of his laboratory work is related to the ultrastructural features of vitreoretinal diseases and to the changes of the inner retina induced by vitreoretinal surgery. Dr. Gandorfer has passed fellowships at the Vitreoretinal Unit of Moorfields Eye Hospital, London, United Kingdom, and at the Pathology Department of the

References (43)

R. Klein et al.
The Wisconsin Epidemiologic Study of Diabetic Retinopathy XVThe long-term incidence of macular edema
Ophthalmology
(1995)
J.C. Javitt et al.
Cost effectiveness of current approaches to the control of retinopathy in type I diabetes
Ophthalmology
(1989)
C.M. Lee et al.
Modified grid laser photocoagulation for diffuse diabetic macular edemalong-term visual results
Ophthalmology
(1991)
G.H. Bresnick
Diabetic macular edemaA review
Ophthalmology
(1986)
C.L. Schepens et al.
Role of the vitreous in cystoid macular edema
Surv Ophthalmol
(1984)
J. Sebag
Diabetic vitreopathy
Ophthalmology
(1996)
F.P. Nasrallah et al.
The role of the vitreous in diabetic macular edema
Ophthalmology
(1988)
T. Hikichi et al.
Association between the short-term natural history of diabetic macular edema and the vitreomacular relationship in type II diabetes mellitus
Ophthalmology
(1997)
H. Lewis et al.
Vitrectomy for diabetic macular traction and edema associated with posterior hyaloidal traction
Ophthalmology
(1992)
H. Lewis
The role of vitrectomy in the treatment of diabetic macular edema
Am J Ophthalmol
(2001)

J.W. Harbour et al.

Vitrectomy for diabetic macular edema associated with a thickened and taut posterior hyaloid membrane

Am J Ophthalmol

(1996)

P.K. Kaiser et al.

Macular traction detachment and diabetic macular edema associated with posterior hyaloidal traction

Am J Ophthalmol

(2001)

S.D. Pendergast et al.

Vitrectomy for diffuse diabetic macular edema associated with a taut premacular posterior hyaloid

Am J Ophthalmol

(2000)

T. Ikeda et al.

Attached posterior hyaloid membrane and the pathogenesis of honeycombed cystoid macular edema in patients with diabetes

Am J Ophthalmol

(1999)

N. Tachi et al.

Vitrectomy for diffuse macular edema in cases of diabetic retinopathy

Am J Ophthalmol

(1996)

T. Yamamoto et al.

Vitrectomy for diabetic macular edemathe role of posterior vitreous detachment and epimacular membrane

Am J Ophthalmol

(2001)

A. Gandorfer et al.

Indocyanine green selectively stains the internal limiting membrane

Am J Ophthalmol

(2001)

S. Kishi et al.

Clinical manifestations of posterior precortical vitreous pocket in proliferative diabetic retinopathy [see comments]

Ophthalmology

(1993)

S.D. Schwartz et al.

Recognition of vitreoschisis in proliferative diabetic retinopathyA useful landmark in vitrectomy for diabetic traction retinal detachment

Ophthalmology

(1996)

C.W. Hamilton et al.

A transmission and scanning electron microscopic study of surgically excised preretinal membrane proliferations in diabetes mellitus

Am J Ophthalmol

(1982)

A.P. Appiah et al.

A review of 324 cases of idiopathic premacular gliosis

Am J Ophthalmol

(1988)

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Citation Excerpt :
Moreover, ultrastructural and immunocytochemical findings correlated neither with HRD nor with DRIL or EZ defects. In accordance with previous studies on epiretinal pathology in diffuse DME,11,13 we found multilayered membranes mainly composed of hyalocytes and myofibroblasts that were embedded in masses of collagen. Fibrous long-spacing collagen within vitreous collagen fibrils was seen in 4 eyes only, representing a remodeling process of vitreous cortex that was previously suggested to be age-related.30
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Retrospective cross-sectional study and laboratory investigation.
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All eyes presented pathologic VMI changes irrespective of the OCT classification of DME type or presence of ERM. Composition of fibrocellular membranes at the VMI indicated remodeling of vitreous cortex and transdifferentiation of hyalocytes into myofibroblasts. Our findings might argue for an early surgical intervention in eyes with DME irrespective of the presence of traction formation imaged by SDOCT.
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Original articlesEpiretinal pathology of diffuse diabetic macular edema associated with vitreomacular traction

Purpose

Design

Methods

Results

Conclusions

Section snippets

Methods

Preoperative data

Discussion

Ophthalmology

Ophthalmology

Ophthalmology

Ophthalmology

Surv Ophthalmol

Ophthalmology

Ophthalmology

Ophthalmology

Ophthalmology

Am J Ophthalmol

Am J Ophthalmol

Am J Ophthalmol

Am J Ophthalmol

Am J Ophthalmol

Am J Ophthalmol

Am J Ophthalmol

Am J Ophthalmol

Ophthalmology

Ophthalmology

Am J Ophthalmol

Am J Ophthalmol

Original articles
Epiretinal pathology of diffuse diabetic macular edema associated with vitreomacular traction