Silicone oils are viscous hydrophobic fluid synthetic polymers. The most commonly used silicone oil in ophthalmology is polydimethylsiloxane.1 Early studies reported that silicone fluids are well tolerated by ocular tissues. However, most of the studies demonstrated adverse effects, including keratopathy, cataract formation, glaucoma, and retinopathy.2 Cataract formation is the most common well-documented complication of injecting silicone oil into the human eye.3 The effect is thought to be due to prevention of normal metabolic exchange through contact of the silicone globule with the posterior lens capsule.4 Due to its potential toxicity, it is recommended that silicone oil be used only for temporary endotamponade and it should be removed when it is no longer needed to keep the retina attached.2
The aim of this study was to investigate the electron microscopic findings of the anterior lens capsule in vitrectomized eyes with silicone oil tamponade. We report the outcome of the 10 eyes that had simultaneous silicone oil removal and phacoemulsification with implantation of acrylic intraocular lenses.
Patients and Methods
This study included 10 eyes of 10 consecutive patients aged 39 to 74 years who had cataract surgery combined with silicone oil removal at our institution between December 2006 and May 2009. Patients who had coexisting ocular disease, severe retinal disease, or inflammatory ocular disease were excluded from the study. A control group of 10 consecutive cases of cataract extraction and intraocular lens implantation in eyes not filled with silicone oil without history of systemic or other ocular disease was included using the same evaluation methods.
Previous vitreoretinal surgery with silicone oil instillation was performed for the following retinal conditions: rhegmatogenous retinal detachment with proliferative vitreoretinopathy (n = 7) and proliferative diabetic retinopathy with nonclearing vitreous hemorrhage associated with tractional retinal detachment (n = 3). The patients underwent vitreoretinal surgery with 20-gauge standard conventional sclerotomies. All surgeries were performed under local anesthesia by retrobulbar injection. For 20-gauge conventional pars plana vitrectomy, the standard three ports of entry were used (upper nasal, upper temporal, and lower temporal quadrants) 3.5 mm posterior to the limbus. All eyes underwent core vitrectomy followed by removal of the posterior hyaloid membrane and vitreous traction. Retinal photocoagulation was performed in selected eyes via a laser. After vitrectomy, the fluid in the vitreous cavity was exchanged with 1,000-centistoke silicone oil in all cases. All injections were performed with the same silicone oil (PDMS; Micromed, Rome, Italy). The standard three ports were closed at the end of the procedure with 7.0 polyglactin 910 sutures. Inferonasal subconjunctival antibiotics and corticosteroids were then injected. Contact to lens was not observed in any case during surgery in the current study. Any eye with a silicone oil bubble in the anterior chamber at any time during surgery and follow-up was excluded. Moreover, patients with observed silicone oil emulsification in the vitreous cavity during follow-up were excluded from the study.
Patients who had a posterior subcapsular cataract formation secondary to intravitreal silicone oil injection on clinical examination were eligible for this study. There were also 10 patients with posterior subcapsular cataracts in the control group. All eyes underwent silicone oil removal and cataract extraction by phacoemulsification with intraocular lens implantation in the same operation. The mean silicone oil removal time was 4.4 ± 1.1 months (range: 3 to 6 months). Surgeries were performed by one surgeon under local anesthesia by retrobulbar injection.
Upper and lower temporal conjunctival incisions were performed. Lower temporal sclerotomy for the infusion cannula was performed and the infusion cannula was inserted. The anterior chamber was irrigated with balanced salt solution to remove possible small silicone bubbles. The anterior chamber was filled with sodium hyaluronate 1.4% (Healon GV; Abbot Laboratories Inc., Abbot Park, IL). An anterior capsulorhexis with a diameter of approximately 4.0 to 5.0 mm was created in the central region of the anterior lens capsule. The anterior capsule was removed and examined with electron microscopy. Phacoemulsification was accomplished through clear corneal incision. An acrylic intraocular lens was implanted in the bag. Upper temporal sclerotomy for removal of silicone oil was performed. The infusion cannula was then opened, and silicone oil was aspirated actively using a syringe. A central posterior capsulotomy was performed in required cases by vitrectomy probe. The fundus was evaluated with the wide field system with indentation of the periphery to ensure that the retina was attached and the silicone oil completely removed. Fluid–air exchange was performed subsequently.
Anterior capsule analysis was performed immediately after surgery. The electron microscopic specialist had no information regarding the patient’s condition. The anterior lens capsules were fixed for 24 hours with 2.5% gluteraldehyde solution and then post-fixed in osmium tetraoxide, dehydrated in increasing concentrations of acetone, air dried, and mounted on metal stubs with a double-sided adhesive band. Then the specimens were sputtered with a 100 Angstrom thick layer of gold in a BIO-RAD sputter apparatus (London, England). After the sputtering procedure, all tissue samples were examined with an LVEM 5 scanning electron microscope (Brno, Czech Republic) and scanning electron micrographs were taken. Anterior lens capsule wrinkles were not observed during the preparation of the tissues.
Statistical analysis of this study was performed by using the Mann–Whitney U test and statistical significance was set at a P value of less than .05. All statistics in this study were analyzed using SPSS for Windows software (SPSS, Inc., Chicago, IL). A written informed consent was taken from all participants. All procedures were conducted in accordance with the Declaration of Helsinki, and informed consent was obtained from all patients.
Of the 10 consecutive patients in this study, 6 were women and 4 were men. The mean age was 59.7 ± 10.8 years (range: 39 to 74 years). The mean follow-up period was 10.6 ± 3.4 months (range: 6 to 16 months). The left eye was affected in 6 cases and the right eye was affected in 4 cases. The control group consisted of 10 eyes without silicone oil that underwent cataract extraction by phacoemulsification with intraocular lens implantation. The mean age was 57.2 ± 9.3 years (range: 43 to 70 years). There were 4 women and 6 men in this group. The left eye was affected in 5 cases and the right eye was affected in 5 cases. There were no statistically significant differences between the two groups for any of the demographic variables examined, including gender and age (P > .05).
All patients had posterior subcapsular cataract. During the follow-up period, no visible silicone oil migration to the anterior chamber occurred in any of the cases. Visible particles of silicone oil in the anterior chamber angle were not observed. There were also no cases of iris prolapse or loss of iris pigment epithelium during surgery. We performed phacoemulsification with in-the-bag implantation of intraocular lenses in 10 eyes after the silicone oil procedure. Postoperatively, there were no cases of retinal redetachment, corneal endothelial decompensation, or macular edema.
In the scanning electron microscopic examination of the posterior surface of the residual anterior lens capsule, islands of the remaining cuboidal lens epithelial cells were detected in all cases in both groups (Fig. 1). In the silicone oil tamponade group, silicone oil droplets were detected on the posterior surface of the anterior lens capsule in 5 cases (50%) (Fig. 2). However, no silicone oil droplets were present in the control group (Fig. 3). Surface irregularities, pits, and depressions were present in the posterior surface of anterior lens capsules in all cases in the silicone oil tamponade group (Figs. 2 and 4). Posterior surfaces of the anterior lens capsule were regular in the control group (Fig. 2).
Figure 1. Scanning electron micrographs showing the islands of the remaining lens epithelial cells (E) on the posterior surface of the residual anterior lens capsule (C) in the (A) silicone oil tamponade group and (B) control group.
Figure 2. Scanning electron micrographs showing silicone oil droplets (*) and pits and depressions (D) on the posterior surface of the anterior lens capsules in the silicone oil tamponade group.
Figure 3. Scanning electron micrographs showing the ultrastructurally normal anterior lens capsular surface in the control group.
Figure 4. Pits and depressions (D) in the silicone oil tamponade group.
Cataract following vitreoretinal surgery results from accidental mechanical injury to the lens or from the untoward physiologic effects of infusion solutions or intraocular tamponades.5 Three different mechanisms have been hypothesized for cataract formation (ie, lens opacities caused by abnormal cell arrangement, altered cell structure and lens opacities, or altered membrane function of the lens epithelial cells).6 Vitreoretinal procedures may also accelerate the development of nuclear sclerotic cataract, probably as a consequence of the greater vulnerability of the aged lens to chemical and mechanical trauma.7
Silicone oil is the most commonly used tamponade for the management of complex retinal detachments. Postoperative anterior segment complications have been reported after silicone oil injection, such as cataract, glaucoma, and keratopathy, even after successful reattachment of the retina.8 Silicone oil has a lower surface tension than gas, and eventually it can emulsify. Moreover, silicone oil injection necessitates its removal, obligating the patient to another operative procedure. Cataract is probably inevitable in eyes permanently filled with silicone oil.9 However, there is some evidence that cataract may not develop if silicone oil remains in the eye only temporarily.10 In eyes with reasonably good visual potential, subsequent cataract extraction can be performed, often with good results.4 Cataract formation leads not only to deterioration of the patients’ vision, but also to impairment of fundus visualization. Therefore, if cataract surgery becomes necessary, it should be performed maintaining the silicone oil tamponade. The most suitable technique under this condition is phacoemulsification with avoidance of damage to the posterior capsule and zonules.11 The most common variety of cataract formation in silicone oil-filled eyes is posterior subcapsular opacification.12 Accordingly, patients who exhibited posterior subcapsular cataract were included in our study. Posterior subcapsular cataract formation has also been observed in senile, complicated, and steroid-induced cataracts.13 Two studies postulated that silicone oil obstructs the normal metabolic exchange of oxygen and nutrients at the silicone oil–tissue interface,14,15 similar to another study in which the author suggested that the silicone cataract is malnutritional, due to inhibition of lens metabolism that results in using anaerobic glycolysis.16 This is in contrast to the occurrence or progression of nuclear cataract after simple vitrectomy without silicone oil instillation, which is attributed to multiple factors, including longer operating time, the distance of the infusion port from the lens, the type of irrigating fluid used, and a surgical technique that spares the anterior vitreous behind the lens.17,18
Emulsification of the silicone oil probably depends on the relative purity of silicone oils. Federman and Schubert19 reported an incidence of emulsified silicone oil in 6% of treated eyes at 3 months after oil injection and this increased to 85% at 6 months. If 1,000-centistoke silicone oil is used, even if it is highly purified, tiny oil droplets that are the precursors of gross emulsification are present in 100% of cases at 1 year.20 Microdroplets in the anterior chamber fluid and small creamy areas of emulsification observed in the superior equatorial retina are the earliest form of emulsification. Ocular fluid motion with instability at the interface leads to formation and separation of tiny droplets.20 There was no emulsified silicone oil in the vitreous cavity and anterior chamber in the current study.
Alazemi et al.21 showed the direct migration of liquid silicone oil from the breast to the mediastinum. Furthermore, Wenkel and Naumann22 reported retrolaminar changes in the optic nerve after silicone oil instillation with secondary angle-closure glaucoma. They postulated the posterior migration of silicone oil into the orbital optic nerve cannot be excluded after long-term silicone oil tamponade. Eckardt et al.23 found single intraretinal macrophages containing silicone oil in eyes injected with silicone oil for 2 years and showed that the retina had multiple defects in the internal limiting membrane. Ohira et al.24 showed that emulsified silicone oil injected into rabbit eyes appeared in the inner retinal layers as early as 1 week after the injection. Leaver et al.14 reported the presence of silicone oil particles in the angle of the anterior chamber, but the incidence of raised intraocular pressure was not high and did not usually appear to be related to the presence of oil in the angle. On gonioscopy, emulsified silicone oil in the anterior chamber angle was not observed in our study.
The lens capsule is freely permeable to water, ions, other small molecules, and proteins with a low molecular weight.25 Intermediate sized molecules present in the aqueous and vitreous humors are required for proper growth and development of the lens and must transit the lens capsule.26 Further, the lens produces proteins that must be released into the humors for appropriate development and homeostasis of the remainder of the eye. The lens capsule is thought to be selectively permeable to these molecules with the rate of their passage influenced by their size and charge.26 The distribution of heparan sulfate side chains and free carboxyl groups within the capsule matrix gives it a net anionic charge.27 Partial masking or removal of these anionic sites in basement membranes results in an increase in permeability.28
In mature cataract, the lens capsule may become more permeable and allow lens proteins to leak out of the lens. Diabetes mellitus also induces changes in the permeability of the lens capsule.29 In our study, we observed the silicone oil droplets on the posterior surface of the anterior lens capsule in 50% of cases. Three explanations may account for this picture. First, permeability of the lens capsule may be increased by changing the molecular charge of the capsule. Our data lead to the conclusion that molecular charge has a significant contribution to a molecule’s diffusion rate through the lens capsule. Second, cataract formation may affect the lens capsule permeability. Third, uncontrolled diabetic condition may influence the permeability of the lens capsule. Three of our 5 patients (60%) with silicone oil droplets on the posterior surface of the lens capsule had been diagnosed as having proliferative diabetic retinopathy and tractional retinal detachment. We did not consider the contamination of capsulorhexis material with nonvisible emulsified silicone oil droplets in the anterior chamber due to the anterior chamber irrigation with balanced salt solution before cataract surgery and did not observe silicone oil bubble in the anterior chamber during follow-up.
Cuboidal lens epithelial cell islands on the posterior surface of the anterior capsule were inevitable after the capsulorhexis. In all cases examined, small islands of equatorial lens epithelial cells were found in both groups.
Most previous studies have shown that the posterior lens capsule and residual anterior capsule change in eyes filled with silicone oil. Miyamoto et al.30 examined the histology of the posterior surface of the anterior capsule following lensectomy and vitrectomy with or without silicone oil tamponade in rabbits by using light and electron microscopy. Ultrastructural examination revealed the presence of many vacuoles amid matrix accumulation on the capsular surface, suggesting the deposition of emulsified silicone oil droplets. Saika et al.31 examined the residual anterior capsules of vitrectomized eyes after pars plana vitrectomy and lensectomy that had been tamponaded with silicone oil. They found that spaces occupied by silicone oil deposits in the extracellular matrix were associated with capsule opacification.
Koch et al.32 investigated the mechanical difficulties of anterior capsulorhexis in vitrectomized eyes filled with silicone oil. They described patches of multilayer epithelial cells with interspersed capsule material on the inner and outer surface of the anterior lens capsule. The development of the anterior subcapsular tissue plaque was explained not only by the proliferative vitreoretinopathy process or by side effects of the surgical procedure, but also by the silicone oil tamponade.
Spraul et al.33 examined the surgically excised posterior lens capsule of eyes with posterior subcapsular cataract filled with silicone oil. Their examination revealed the presence of spindle-like cells surrounded by basement membrane associated with a fibrillary substance and collagen fibers. They termed this phenomenon posterior fibrous pseudometaplasia of lens epithelium because posterior migration of lens epithelial cells followed production of collagen in these cells.
No previous study included examination of the anterior lens capsule in vitrectomized eyes with silicone oil tamponade. In the current study, we identified surface irregularities, pits, and depressions under the anterior lens capsule in both groups. Therefore, we suggest that this appearance was the effect of fibrous pseudometaplasia of the lens epithelium rather than silicone oil bubble. These observations are in accordance with the study of Spraul et al.33 We propose that lens epithelial cells initially produce collagen under the anterior lens capsule and then migrate to the posterior capsule.
Our study revealed surface irregularities under the anterior lens capsules in all cases and silicone oil particles under the anterior lens capsule in 50% of cases with silicone oil tamponade, which has not been described previously. Further studies with larger patient groups are needed to confirm our findings.
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- Pesin SR, Olk RJ, Grand MG, et al. Vitrectomy for premacular fibroplasia: prognostic factors, long-term follow-up and time course of visual improvement. Ophthalmology. 1991;98:1109–1114.
- McCuen BW, de Juan EJ, Landers MB, Machemer R. Silicone oil in vitreoretinal surgery: Part 2. Results and complications. Retina. 1985;5:198–205. doi:10.1097/00006982-198500540-00002 [CrossRef]
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- Casswell AG, Gregor ZJ. Silicone oil removal: I. The effect on the complications of silicone oil. Br J Ophthalmol. 1987;71:893–897. doi:10.1136/bjo.71.12.893 [CrossRef]
- Larkin GB, Flaxel CJ, Leaver PK. Phacoemulsification and silicone oil removal through a single corneal incision. Ophthalmologe. 1998;105:2023–2027. doi:10.1016/S0161-6420(98)91119-8 [CrossRef]
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- Leaver PK, Grey RHB, Garner A. Silicone oil injection in the treatment of massive preretinal retraction: I. Late complications in 93 eyes. Br J Ophthalmol. 1979;63:361–367. doi:10.1136/bjo.63.5.361 [CrossRef]
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- De Bustros S, Thompson JT, Michels RG, Enger C, Rice TA, Glaser BM. Nuclear sclerosis after vitrectomy for idiopathic epiretinal membrane. Am J Ophthalmol. 1988;105:160–164.
- Yamasaki A, Nagata M, Takagi S, Tamai A. Time-course of lens opacity and morphological changes in rabbit lens epithelial cells after intravitreal silicone oil injection. Jpn J Ophthalmol. 1994;38:116–122.
- Federman JL, Schubert HD. Complications associated with the use of silicone oil in 150 eyes after retina vitreous surgery. Ophthalmology. 1988;95:870–876.
- Hammer ME. Vitreous substitutes. In: Tasman W, Jaeger EA, eds. Duane’s Clinical Ophthalmology on CD-ROM. Philadelphia: Lippincott, Williams & Wilkins; 2006:1–46.
- Alazemi S, Suarez MM, Baier HJ. Direct migration of liquid silicone oil to the mediastinum. Am J Med. 2008;121:e3–e4. doi:10.1016/j.amjmed.2007.06.034 [CrossRef]
- Wenkel H, Nauman GO. Retrolaminar infiltration of optic nerve with intraocular tamponade following silicone oil infiltration. Klin Monatsabl Augenheilkd. 1999;214:120–122. doi:10.1055/s-2008-1034762 [CrossRef]
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- Miyamoto T, Saika S, Yamanaka A, Okada Y, Ohnishi Y. Deposition of silicone oil droplets in the residual anterior lens capsule after vitrectomy and lensectomy in rabbits. Br J Ophthalmol. 2004;88:703–707. doi:10.1136/bjo.2003.021113 [CrossRef]
- Saika S, Miyamoto T, Tanaka T, Ohnishi Y, Oshima A, Kimura W. Histopathology of anterior lens capsules in vitrectomized eyes with tamponade by silicone oil. J Cataract Refract Surg. 2002;28:376–378. doi:10.1016/S0886-3350(01)00957-9 [CrossRef]
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- Spraul CW, Jakobczyk-Zmija MJ, Aigner T, Lang GK. Posterior fibrous pseudometaplasia of lens epithelial cells in phakic eyes filled with silicone oil. Graefes Arch Clin Exp Ophthalmol. 2002;240:829–834. doi:10.1007/s00417-002-0563-y [CrossRef]