Comparative Assessment of Intraocular Inflammation Following

Acta Ophthalmologica 2019

Comparative assessment of intraocular inﬂammation following standard or heavy silicone oil tamponade: a prospective study

Francesco Semeraro,1 Andrea Russo,1 Francesco Morescalchi,1 Elena Gambicorti,1 Sara Vezzoli,2 Francesco Parmeggiani,3 Mario R. Romano4 and Ciro Costagliola5

1Department of Medical and Surgical Specialties, Radiological Sciences and Public Health, University of Brescia, Brescia, Italy 2Department of Medical and Surgical Specialties, Radiological Sciences and Public Health – Section of Legal Medicine, University of Brescia, Brescia, Italy 3Department of Ophthalmology, University of Ferrara, Ferrara, Italy 4Department of Biomedical Sciences, Humanitas University, Milan, Italy 5Department of Medicine and Health Sciences, University of Molise, Campobasso, Italy

ABSTRACT. vitreous substitute (Cibis et al. 1962). Purpose: To evaluate the inflammation associated with the use of standard The use of a vitreous substitute that is silicone oil (polydimethylsiloxane; PDMS) and heavy silicone oil (HSO) heavier than water has been recently Densiron-68TM in patients undergoing vitrectomy for retinal detachment. suggested for use as an intraocular Materials and Methods: A prospective study was performed involving 35 patients tamponade in surgical cases of compli- scheduled to undergo vitrectomy for retinal detachment. Patients received PDMS cated retinal detachment of the inferior or Densiron-68TM HSO according to superior or inferior retinal localization of the quadrants (Azen et al. 1998). To date, three groups of heavy tamponades have tears, respectively. For assessing the inflammation, prostaglandin E2 (PGE2) and interleukin-1a (IL-1a) levels were evaluated in the aqueous. been introduced into surgical practice: Results: Thirty-five eyes of 35 patients completed the study: 20 eyes received fluorinated silicone oil or fluorosilicone, perfluorocarbon liquids and semifluori- HSO, and 15 eyes received PDMS. The mean aqueous PGE2 level was Æ nated alkanes, such as perfluorohexy- significantly higher in HSO patients than in PDMS patients (869.16 loctane (F H ) (Morescalchi et al. Æ < 6 8 242.83 pg/ml versus 369.38 209.7 pg/ml, respectively; p 0.0001). The mean 2014). Densiron-68TM is a commonly aqueous IL-1a level was also significantly higher in HSO patients than in PDMS used solution comprising F6H8 and patients (81.40 Æ 36.9 pg/ml versus 40.8 Æ 32.5 pg/ml, respectively; p = 0.002). 5000c silicone oil, with a specific gravity In HSO, a moderate positive correlation between the endotamponade duration and of 1.06 and a viscosity of 1387 mPas. both PGE2 (r = 0.44; p = 0.05) and IL-1a (r = 0.48; p = 0.033) levels was According to the evidence reported observed. In PDMS, a strong positive correlation between the endotamponade in the literature, the heavy tamponades duration and both PGE2 (r = 0.89; p < 0.0001) and IL-1a (r = 0.68; p = 0.006) are more prone to cause intraocular levels was observed. inflammation compared with standard Conclusion: Although both HSO and PDMS yielded favourable success rates in silicone oil, especially if they remain in the surgical treatment of complicated retinal detachments, HSO triggered a the eye for several months (Morescal- more severe inflammatory reaction, in a time-dependent manner. chi et al. 2014). Side-effects of heavy silicone oil (HSO) are associated with the chemical and physical properties of Key words: heavy silicone oil – inflammation – retinal detachment – standard silicone oil – vitrectomy the tamponading compound and are similar to those associated with conventional silicone oil (Semeraro et al. Acta Ophthalmol. 2019: 97: e97–e102 2014). Four main mechanisms are ª 2018 Acta Ophthalmologica Scandinavica Foundation. Published by John Wiley & Sons Ltd reported in the genesis of the inflam- doi: 10.1111/aos.13830 matory reaction to standard and HSO: direct toxicity and immunogenicity, Introduction substitute in vitreoretinal surgery over toxicity due to impurities or instability Introduced in 1962, silicone oil has been the past 50 years, and to date, it remains of the agent, oil emulsification and the most commonly used vitreous the only widely accepted long-term mechanical injury due to gravity

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(Mackiewicz et al. 2007). However, the PDMS silicone oil (100% PDMS; den- Table 1. Patient demographics and baseline inflammation associated with HSO sity 970 kg/m3; Alchimia Srl, Ponte characteristics. appears to be due to a delayed type San Nicolo, PD, Italy), and 20 eyes TM HSO PDMS IV hypersensitivity reaction and varies received HSO Densiron-68 (mixture (N = 20) (N = 15) greatly because the duration of appli- of 69.5% ultrapure PDMS and 30.5% cation significantly affects the level of perfluorohexyloctane; viscosity of Age: mean 62.3 (16.7) 58.9 (12.8) inflammation in the eye (Morescalchi 1200 cSt and density of 1040 kg/m3; (SD), years et al. 2014). Fluoron GmbH, Ulm, Germany) Sex: n (%) For the safe and effective use of according to superior or inferior retinal Men 15 (75) 11 (73) retinal tamponades, an awareness of localization of the tears, respectively Women 5 (25) 4 (27) Lens status (%) their physical, chemical and inflamma- (Table 2). Phakic 10 (50) 6 (40) tory properties is a prerequisite; vitre- All phakic patients were operated Pseudophakic 10 (50) 9 (60) oretinal surgeons select the most with phacoemulsification of the crys- Preoperative 0.15 (0.12) 0.14 (0.09) suitable tamponade on the basis of talline lens plus intraocular lens (IOL) visual this knowledge. In this study, we implant at the time of vitrectomy to acuity: mean prospectively evaluated the inflamma- allow a careful cleaning of the vitre- (SD), decimal tion associated with both 1000 cSt ous base. Vitrectomy surgery was HSO = heavy silicone oil, PDMS = poly- silicone oil (100% polydimethylsilox- performed using a 23-gauge transcon- dimethylsiloxane, SD = standard deviation. ane; PDMS) and 1200 cSt HSO (Den- junctival system, and no triamcinolone siron-68TM) in patients undergoing was used during any step of the vitrectomy for retinal detachment. To surgery. determination of prostaglandin E2 the best of our knowledge, this is the After the removal of the posterior (PGE2) levels. Analyses were performed first study designed to compare the hyaloids, the vitreous base was thor- using Dynex Technologies DSXTM (v. inflammatory complications associated oughly removed. All visible proliferative 6.03; Chantilly, VA, USA) according to with Densiron-68TM and standard sili- vitreoretinopathy (PVR) membranes the manufacturer’s instructions. Briefly, cone oil. were dissected, and relaxing retino- the analysis was based on the competi- tomies were performed, in two eyes, in tion between PGE2 and PGE2-acetyl- Materials and Methods the inferior retina of PDMS group. The cholinesterase conjugate (AChE; PGE2 retinal periphery was inspected for reti- tracer) for a limited amount of PGE2 This study was conducted at the nal breaks that were marked with endo- monoclonal antibody. As the concen- University Eye Clinic of ‘Spedali diathermy, after that the retina was tration of the PGE2 tracer was constant Civili di Brescia’ in accordance with reattached using perfluorocarbon liquid while the concentration of PGE2 sam- the ethical principles of the Declara- and air. Three rows of endolaser treat- ples varied, the amount of PGE2 tracer, tion of Helsinki. The Ethics Commit- ment were applied behind the posterior which was able to bind to the PGE2 tee of Spedali Civili di Brescia (Italy) vitreous base in all patients (200 spots, monoclonal antibody, was inversely approved the study protocol (regis- 200–250 mW according to retinal pig- proportional to the concentration of tered with clinicaltrials.gov, identifier mentation). Finally, after a complete PGE2 in the well. NCT02361645). All study participants perfluorocarbon liquid-to-air exchange, The interleukin-1a (IL-1a) assay was provided written informed consent. the eye was filled with PDMS or Den- based on a double-antibody ‘sandwich’ This was a prospective study includ- siron-68TM according to tear localiza- technique. Each well of the microtiter ing 35 eyes of 35 patients consecutively tion. All patients in both groups were plate supplied with the kit was coated enrolled from September 2015 to prescribed topical dexamethasone (six with a monoclonal antibody specific March 2016; the patients were sched- times per day) and homatropine (two for IL-1a. This antibody can bind to uled to undergo 23-gauge, three-port times per day). any IL-1a introduced into the well. An pars plana vitrectomy for retinal Both PDMS and HSO were AChE that binds selectively to a dif- detachment, and all patients completed removed using a 23-gauge instrument. ferent epitope on IL-1a was also added the study. Inclusion criteria were age Patients with PDMS were positioned in to the well, forming a ‘sandwich’ by ≥18 years and retinal detachment with prone position for 2 hr before the binding on opposite sides of the IL-1a multiple or giant breaks, such as it surgery, while patients with HSO were molecule. The concentration of the requires the tamponade with silicone maintained in supine for the same analyte was then determined by mea- oil. The exclusion criteria were diabetes amount of time. At the beginning of suring the enzymatic activity of the mellitus, previous vitrectomy in the the surgery, 0.5–1.0 ml of undiluted AChE by adding Ellman’s reagent to study eye, previous buckle surgery, aqueous was removed before opening each well. previous intravitreal injection, concur- the infusion. Samples were immediately rent retinovascular or other ocular frozen and stored at À40 °C until Statistical analysis inflammatory disease, history of ocular analysis. trauma and concomitant intake of any Descriptive statistics were used to pre- topical or systemic NSAID or corti- sent demographic and ocular baseline Measurements of prostaglandin E2 and costeroid therapy. characteristics. An independent-sam- interleukin-1a levels Patient demographics and baseline ples t-test was performed to determine characteristics are listed in Tables 1 Vitreous samples were defrosted whether there were differences in PGE2 and 2. Fifteen eyes received 1000 cSt and subjected to semiquantitative and IL-1a levels between the PDMS e98 Acta Ophthalmologica 2019

Table 2. Anatomical and clinical characteristics at baseline. combined surgery with phacoemulsiﬁ- cation. HSO (N = 20) PDMS (N = 15) p value The mean aqueous PGE2 level Æ Phakic/pseudophakic 13/7 9/6 1 was 869.16 242.83 pg/ml in HSO No. of breaks 1.65 Æ 0.67 1.73 Æ 0.70 0.725 patients, which was higher than that Location of breaks (clock hours) 4–89–3 – in PDMS patients (369.38 Æ 209.7 pg/ Macula status on/oﬀ 11/9 7/8 0.738 ml; p < 0.0001). Similarly, the mean Duration of detachment (days) 4.15 Æ 1.7 4.2 Æ 1.9 0.94 aqueous IL-1a level was higher in HSO PVR patients (81.40 Æ 36.9 pg/ml) than in A65– Æ – PDMS patients (40.8 32.5 pg/ml; B32= C(1–4) 11 8 – p 0.002). There was a moderate positive HSO = heavy silicone oil, PDMS = polydimethylsiloxane, PVR = proliferative vitreoretinopathy. correlation between the endotamponade duration and both PGE2 (r = 0.44; p = 0.05) and IL-1a (r = 0.48; Table 3. Anatomical and functional outcomes at the time of oil removal. p = 0.033) levels in HSO patients (Fig. 1). Similarly, in PDMS patients, N = N = HSO ( 20) PDMS ( 15) there was a strong positive correlation Retinal reattachment: n (%) 18 (90) 12 (80) between the endotamponade duration r = < Visual acuity: mean (SD), decimal 0.26 (0.15) 0.28 (0.1) and both PGE2 ( 0.89; p 0.0001) IOP: mean (SD), mmHg 22.1 (5.1) 19.5 (6) and IL-1a levels (r = 0.68; p = 0.006; Requiring IOP treatment: n (%) 20 (100) 9 (60) Fig. 2). Microemulsion of silicone in AC: n (%) 20 (100) 10 (67) Posterior synechiae: n (%) 15 (75) 7 (47) Endotamponade period: mean (SD), weeks 12.8 (4.8) 12.3 (6.2) Discussion

AC = anterior chamber, HSO = heavy silicone oil, IOP = intraocular pressure, PDMS = poly- This prospective study evaluated the dimethylsiloxane, SD = standard deviation. inflammation associated with standard silicone oil (PDMS) and the HSO Densiron-68TM in patients undergoing and HSO groups. The sample size of 35 from 0.15 Æ 0.12 (decimal scale) to vitrectomy for retinal detachment. patients provided a power of 0.81, for 0.26 Æ 0.15 in the HSO group and Results show that the intraocular demonstrating an effect size of 0.87 from 0.14 Æ 0.09 to 0.28 Æ 0.1 in the inflammatory reaction is greater in eyes between the two groups, at a signifi- PDMS group (p < 0.001, for both filled with HSO compared with PDMS. cance level of 0.05. A Pearson’s pro- groups). This inflammation significantly corre- duct–moment correlation was run to An increase in intraocular pressure lated with the endotamponade dura- assess the relationship between both (IOP) >25 mmHg was noted in all tion in both groups; this positive PGE2 and IL-1a levels and the dura- HSO patients in the 3-month follow- correlation further supports the evi- tion of the ocular endotamponades. All up before oil removal. All cases were dence of side-effects when silicone oil is statistical analyses were performed controlled with topical combination of used for a long period (Theelen et al. using SPSS software v. 20 (IBM Corp, 0.5% timolol and 2% dorzolamide. 2004; Stappler et al. 2011; Morescalchi Armonk, NY, USA). p < 0.05 was Three patients required the addition et al. 2014; Schwarzer et al. 2014). To considered statistically significant. of 0.004% travoprost at bedtime, and our knowledge, this is the first report one patient required a short course of on a direct comparison between the Results oral acetazolamide, after experiencing inflammatory outcomes of standard a peak IOP of 35 mmHg. In the PDMS silicone oil and HSO. Heavy silicone oil (HSO) and PDMS group at the 3-month follow-up, IOP The stability and immunological patients underwent the removal of the was controlled in nine eyes (60%) with tolerability of PDMS make it relatively intraocular tamponade agent after a a topical combination of 0.5% timolol safe as a long-term internal tampon- mean (Æstandard deviation) period of and 2% dorzolamide or 0.004% travo- ade. Histological examination of the 12.8 Æ 1.1 and 12.3 Æ 0.6 weeks, prost, while six eyes (40%) did not human retina after more than 3 years respectively (p = 0.17). In the HSO require IOP-reducing therapy. of PDMS endotamponade did not group, at the time of oil removal, During the surgery for oil removal, show significant morphological alter- anatomical success was achieved in 18 in all patients treated with HSO and in ations; however, intraretinal or intra- eyes (90%), while recurrence of retinal 10 patients (67%) treated with PDMS, cellular deposits suggestive of silicone detachment was present in two eyes a microemulsion of silicone oil was might be observed in attached retinas (10%; Table 3). These two eyes observed in the anterior chamber. (Kirchhof et al. 1986). required further surgery. In the PDMS Moreover, posterior synechiae between Heavy silicone oils (HSOs) are group, anatomical success was the iris and the IOL were observed in derived from a mixture of a highly achieved in 12 eyes (80%). Three 15 eyes (75%) filled with HSO and in viscous PDMS (>5000 mPas) and dif- eyes (20%) required further surgical seven eyes (47%) filled with PDMS ferent semifluorinated alkanes (F6H8, procedures. The best-corrected visual (Table 3). Posterior synechiae were F4H5 and F4H6), or a similar substance acuity (BCVA) significantly improved present in all eyes that underwent (RMN-3, a partly fluorinated olefin),

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substances previously used intraopera- tively (PFCL, remnants of oil or vitreous) and especially by the oil/aqueous movement generated by eye move- ments resulting in shearing forces (Savion et al. 1996; Morescalchi et al. 2014; Semeraro et al. 2014). Microemulsion is suspected to trigger chemotaxis of inflammatory cells and phagocytosis that stimulate a foreign body-type reaction and consequent phagocytosis by macrophages. This possibility is supported by the observation of macrophages originat- ing in the immune response, as these are the white cells most commonly represented in the inflammatory infil- Fig. 1. Scatterplot of the moderate linear relationship between endotamponade duration and both trate (Zeana et al. 1999; Vote et al. PGE2 and IL-1a levels with heavy silicone oil. Blue rhombuses represent PGE2, and red squares represent IL-1a. Solid line represents PGE2 trendline, and dashed line represents IL-1a trendline. 2003). Moreover, immunoglobulin or IL-1a = interleukin-1a; PGE2 = prostaglandin E2. fractions of complement have been reported to be detectable on the surface of the vitreous substitute months after silicon oil expositions (Morescalchi et al. 2014). Therefore, the inflammation associated with HSO appears to be due to a delayed type IV hypersensitivity reaction. This is consistent with the significant correlation between inflammation and duration of the endotamponade found in the present study. In turn, intraocular inflammation promotes early emulsification of the endotamponade (Kociok et al. 2005), and the consequent diffusion of molecules from the endotamponade promotes further inflammation. There- fore, emulsification is probably both the effect and the cause of the intraocular inflammation, while individual agents might be a stimulant for inflammatory reaction (Majid et al. 2008). The rate of postoperative inflamma- TM Fig. 2. Scatterplot reporting the strong linear relationship between endotamponade duration and tion associated with Densiron-68 both PGE2 and IL-1a levels with standard silicone oil. Blue rhombuses represent PGE2; red varies greatly across different trials, squares represent IL-1a. Solid line represents PGE2 trendline; dashed line represents IL-1a depending mostly on the tamponade trendline. IL-1a = interleukin-1a; PGE2 = prostaglandin E2. duration. Sandner and Engelmann (Sandner & Engelmann 2006) evaluated the intraocular adverse effects and these have a lower tendency to dispersion and emulsification. Our after a 3-month endotamponade with create dispersion and emulsion. How- results show that silicone oil tends to Densiron-68TM and reported a mild-to- ever, the concentration of the two stimulate inflammation in a time- moderate anterior chamber reaction, components may vary with time and dependent manner and that HSO is mainly during the first postoperative temperature, and potential chemical more inflammatory than standard sili- days, accompanied by flaring in the decomposition of HSO has been cone oil. This could be partially anterior chamber with possible fibrin reported (Banaee 2012; Morescalchi explained by a mild separation of exudation. Banaee (2012) reported a et al. 2014) where the heavier compo- Densiron-68TM in polymethylsiloxane case of massive reaction in the anterior nent tends to settle over time in the and F6H8, leading to microemulsion chamber, with an associated deposition inferior part of the bubble, separating of the latter. Heavy silicone oil (HSO) of oil globules behind the cornea, and from PDMS. As previously reported, demerger and emulsification are also iris depigmentation, together with pig- Densiron-68TM is a mixture of 30.5% stimulated by the presence of red blood ment globules both on the iris and F6H8 and 69.5% polymethylsiloxane cells, plasma lipoproteins, apolipopro- floating in the anterior chamber. A and possesses a high viscosity to reduce teins, encircling bands and other time-dependent inflammatory reaction e100 Acta Ophthalmologica 2019 is consistent with a study by Auriol these small droplets might induce a HSO triggered a higher inflammatory et al. (2008) in which authors reported mild chronic reaction in which the reaction, mainly due to its emulsifica- a high rate of inflammatory reactions macrophages react towards the tam- tion tendency, and the extent of the (40.7%) associated with a long ponade emulsion as a foreign body. inflammation appeared to be propor- (>6 months) persistence of Densiron- Therefore, they are able to promote iris tional to the duration of tamponade 68TM. synechiae and increase IOP. Moreover, application. In particular, our study It is quite difficult to differentiate PGE1 and PGE2 increase IOP by showed that the PGE2 and IL-1a between inflammation caused by the inducing vasodilatation and increasing aqueous levels were more than double endotamponade and the inflammatory the permeability of the blood–aqueous in eyes with HSO compared to those in reaction associated with the underlying barrier (Semeraro et al. 2015). eyes with PDMS. In conclusion, as retinal diseases. However, the inflam- It has been also reported, from a indicated by our results, the retention mation has been proved to be related to systematic review of randomized clinical time of HSO should be kept short and the immunogenicity of the compounds trials, a trend of ocular hypertension in restricted as much as possible. In and to the surfactants that modify the eye treated with HSO compared to patients scheduled for vitrectomy with interfacial tension (IT) (Savion et al. PDMS (Romano et al. 2015). The silicone oil, IOP should be closely 1996). Regarding the immunogenicity, HSO was associated with significant monitored and IOP-reducing treatment the PDMS droplets induce a macro- higher IOP in the first 2 weeks post-op promptly commenced. Finally, appro- phagic foreign body reaction associ- period when compared with PDMS, priate anti-inflammatory therapy ated with the phagocytosis of PDMS where the difference was not significant with steroidal or non-steroidal anti- emulsion by retinal pigment epithelium at 1 month post-op (Wong et al. 2009). inflammatory drugs, together with (RPE) cells (Wong et al. 2009). This The raised IOP was difficult to treat cycloplegics, should be considered for granulomatous reaction is sustained by (Costagliola et al. 2009). The reason for the duration of the HSO tamponade epithelioid cells that are responsible for an increase of IOP in the early post-op retention. the cascade of inflammation (De may be due higher rate of retinectomy in Queiroz et al. 1992; Morescalchi et al. the HSO group. Retinectomy is gener- 2014). Regarding the surfactants, they ally associated with increased inflam- are amphiphilic compounds extending mation due to the breakdown of blood– References in both oil and water with different ocular barrier and bleeding at the edge Auriol S, Pagot-Mathis V, Mahieu L, Lemoine tails. The surfactants are either biosur- of cut retina (Wong et al. 2009). On the C & Mathis A (2008): Efficacy and safety of factants produced by the eye itself or contrary, the late postoperative increase heavy silicone oil Densiron 68 in the treat- impurity present, as low molecular of IOP in eye treated with HSO is mainly ment of complicated retinal detachment with weight component or other impurities, related to the inflammation induced by large inferior retinectomy. Graefes Arch – during the manufacturing process of the HSO. In fact, the HSO is a solution Clin Exp Ophthalmol 246: 1383 1389. PDMS. The surfactants are able to of semifluorinated alkane and PDMS, Azen SP, Scott IU, Flynn HW, Lai MY, Topping TM, Benati L, Trask DK & Rogus reduce the IT, as cohesion force of a where the F6H8 has low viscosity and LA (1998): Silicone oil in the repair of liquid aiming to increase the ‘wall higher propensity for dispersion (Wong complex retinal detachments. A prospective tensions’, promoting the emulsion of et al. 2005). observational multicenter study. Ophthal- PDMS. As previously reported, HSO is Our study has a few limitations: mology 105: 1587–1597. a mixed compound obtained by adding firstly, the patients were not properly Banaee T (2012): Early decomposition of a semifluorurate (alkane or ether) to randomized, but they received PDMS or retained heavy silicone oil droplets. J Oph- – PDMS. The semifluorurate reduces the HSO according to the clinical practice thalmic Vis Res 7:64 66. IT and also promotes immunogenic (localization of the retinal tear). How- Cibis PA, Becker B, Okun E & Canaan S (1962): The use of liquid silicone in retinal reaction responsible for inflammation ever, there were no differences between detachment surgery. Arch Ophthalmol Chic and emulsion (Hiscott et al. 2001). This groups in terms of PVR or period of 1960: 590–599. is the reason why it is recommended to retinal detachment. Secondly, pha- Costagliola C, dell’Omo R, Romano MR, remove the HSO within 3 months. coemulsification itself can stimulate Rinaldi M, Zeppa L & Parmeggiani F In the current study, IOP appeared inflammation and breakdown of the (2009): Pharmacotherapy of intraocular to be greater in the HSO group with blood–retinal barrier, although pha- pressure: part I. Parasympathomimetic, 100% of patients requiring topical coemulsification procedures were sympathomimetic and sympatholytics. – treatment (untreated IOP >25 mmHg) uneventful and carried out in both Expert Opin Pharmacother 10: 2663 2677. De Queiroz JM, Blanks JC, Ozler SA, Alfaro versus 60% of patients in the PDMS groups. Thirdly, we enrolled a limited DV & Liggett PE (1992): An experimental group. This might be explained by the number of patients. However, despite a study. Retina 12: S33. different tendency for emulsification of relatively high standard deviation in the Hiscott P, Magee RM, Colthurst M, Lois N & the two tamponades. Indeed, HSO is vitreous levels of PGE2 and IL-1a, the Wong D (2001): Clinicopathological corre- known to remain stable for 3 months, statistical significance between PDMS lation of epiretinal membranes and posterior while PDMS 1000 cSt is stable for 3– and HSO is pronounced. lens opacification following perfluorohexy- 6 months (Nguyen et al. 1992; Hiscott In our study, both HSO and PDMS loctane tamponade. Br J Ophthalmol 85: – et al. 2001). This is consistent with the yielded favourable success rates in the 179 183. 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