Clinical StudyThe Effects of Uncomplicated Cataract Surgery on RetinalLayer Thickness

Ali Kurt and Raşit Kılıç

Department of Ophthalmology, Faculty of Medicine, Ahi Evran University, Kırşehir, Turkey

Correspondence should be addressed to Ali Kurt; dralikurt@gmail.com

Received 16 January 2018; Accepted 18 April 2018; Published 5 June 2018

Academic Editor: Marcel Menke

Copyright © 2018 Ali Kurt and Raşit Kılıç. )is is an open access article distributed under the Creative Commons AttributionLicense, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work isproperly cited.

Purpose. Our aim was to assess changes in the total retinal thickness (TRT), total retinal volume (TRV), and retinal layer thicknessafter uncomplicated cataract surgery. Methods. A total of 32 eyes of 32 patients who had undergone uncomplicated phaco-emulsification surgery and intraocular lens implantation in one eye were enrolled. Effective phacoemulsification time (EPT) andtotal energy (TE) were recorded. )ickness and TRV were measured using optical coherence tomography. Data were collectedpreoperatively and at postoperative day 1, 7, 30, 90, and 180. Results. )e study results showed a decrease in TRT, TRV, and mostretinal layer thicknesses at the first postoperative day visit and then increasing at week 1, and months 1 and 3, and then relativelydecreasing at month 6 although not returning to preoperative levels. )e least affected layers were the retinal pigment epitheliumand outer plexiform layer. )ere was a positive correlation between EPTand TE and ganglion cell layer in a 1mm circle and innernuclear layer in a 1–3mm circle (p< 0.05). Conclusion. )e results suggest that long-term follow-up of more than 6 months isnecessary after cataract surgery to see whether total retinal and segmental values return to preoperative levels. )is study wasregistered with Australian New Zealand Clinical Trials Registry (ANZCTR): ACTRN12618000763246.

1. Introduction

Cataract is the most common preventable cause of vision lossworldwide. Pseudophakic cystoid macular edema (PCME),known as Irvine–Gass syndrome, is one of the most commoncomplications after cataract surgery. It is generally subclinicalin most cases and rarely causes vision loss. Although theincidence of clinical PCME has decreased with small incisioncataract surgery and phacoemulsification (PE), it can stillcause unexpected vision loss [1].)e exact pathophysiology ofPCME is not fully understood but seems to be related to theinflammation triggered by surgery. )e inflammatory cyto-kines and mediators break down the blood-retina barrier andresult in increased vascular permeability and cystoid macularedema [2, 3]. Other factors such as posterior capsule rupture,vitreous loss, retained lens fragments, vitreomacular traction,and iris trauma after complicated surgery can also increase thePCME incidence [1–3].

PCME is most commonly seen 4–6 weeks after surgery[1–3]. Fundus fluorescein angiography (FFA) reveals capillarydilatation, leakage from the foveal capillaries, and developingpetalloid appearance. Optical coherence tomography (OCT)is a noninvasive device which enables detection of cysticspaces, retinal thickening, and subretinal fluid. OCT also hasgood repeatability and reproducibility when measuring ret-inal layer thickness at the macula [4]. It is an excellent methodfor monitoring disease activity [3].

)e current knowledge on the effect of postoperativeinflammation on retinal cells and layers is limited. We arenot aware of any study assessing the retinal segments todetect the layers that are most affected by cataract surgerywith long-term follow-up. )e purpose of this study was toevaluate the thickness of each retinal segment quantitativelywith spectral domain (SD)-OCT before and after un-complicated cataract surgery to gain additional informationon PCME.

HindawiJournal of OphthalmologyVolume 2018, Article ID 7218639, 6 pageshttps://doi.org/10.1155/2018/7218639

mailto:dralikurt@gmail.comhttps://www.anzctr.org.au/Trial/Registration/TrialReview.aspx?id=374949&isReview=truehttp://orcid.org/0000-0002-3893-6280http://orcid.org/0000-0001-6671-9067https://doi.org/10.1155/2018/7218639

2. Methods

�is prospective study was conducted at the Ahi EvranTraining and ResearchHospital betweenDecember 2016 andOctober 2017. �e study was approved by the institutionalreview board and adhered to the tenets of the Declaration ofHelsinki. Informed consent was obtained from all the pa-tients. A total of 43 eyes of 43 Caucasian patients who hadundergone uncomplicated cataract surgery and posteriorchamber intraocular lens implantation were included.Eleven patients were excluded due to the lack of follow-upexaminations, and the study was nally conducted on the 32eyes of 32 patients. �e visual acuity was evaluated witha Snellen chart, and a detailed biomicroscopic anterior andposterior segment examination was performed with pupil-lary dilatation. Air pu tonometry was used to measure theintraocular pressure. �e axial length was measured usingoptical low-coherence reectometry (Lenstar LS 900, Haag-Streit AG, Koeniz, Switzerland). Best corrected visual acuitywas 2/20 and higher in all patients preoperatively.

Exclusion criteria consisted of macular pathologies,retinal vascular occlusion, history of any other ocular dis-orders (including uveitis, severe dry eye, eye trauma,glaucoma, and pseudoexfoliation syndrome) or surgery, anysystemic disorders (such as diabetes, hypertension, asthma,or chronic obstructive pulmonary disease), systemic in-ammation (inammatory bowel disease and hepatitis B orC), the current use of any topical or systemic medication oranti-inammatory agent, and intraoperative complicationssuch as posterior capsular rupture, vitreous loss, iris pro-lapse, and low scan quality images due to dense cataract.

Cataract surgery was performed with the Inniti PEdevice (Alcon Inc., Forth Worth, TX, USA) using a torsionalhandpiece. �e stop and chop technique was used in allcases. Eective phaco time and phaco energy were recorded.Postoperatively, all patients were prescribed topical moxi-oxacin and dexamethasone four times a day for three weeksand Nevanac three times a day for four weeks. �e sameauthor (AK) performed all surgeries and examinations.

2.1. OCT Scan Protocol. All subjects underwent pupillarydilatation with 1% tropicamide and 2.5% phenylephrinehydrochloride eye drops prior to imaging. We used the SD-OCT, Spectralis (Heidelberg Engineering, Heidelberg, Ger-many) device with software version 6.3.3.0 in this study as ithas a higher repeatability index [4]. OCT imaging was carriedout using the following parameters: 20°×15° degrees(5.9× 4.4mm), automatic real-time averaging of 100 frames,19 horizontal sections at 240 µm intervals, and 512 A-scansper B-scan. We only included images with a quality higherthan 15 dB in the study. �e image acquisition was followedby automatic intraretinal layer segmentation performed bythe inbuilt Spectralis software to include the retinal nerve berlayer (RNFL), ganglion cell layer (GCL), inner plexiform layer(IPL), inner nuclear layer (INL), outer plexiform layer (OPL),outer nuclear layer (ONL), retina pigment epithelium (RPE),total retinal volume (TRV), and total retina thickness (TRT)(Figure 1). Intraretinal layer thicknesses were obtained for

each ETDRS subeld at a central 1mm circle and 1–3mmcircles that included the superior, temporal, inferior, and nasalsubelds (Figure 2). �e rst Spectralis scan was set asa reference image, and the images during future visits wereacquired with real-time image registration by follow-upmodeby the ophthalmologist. �e ETDRS grid was centered on thefovea manually if it was not positioned correctly automati-cally. We also checked the accuracy of retinal layer seg-mentation in every patient. �e 3–6mm subelds were notincluded as it exceeded the area of our imaging angle. Datawere collected preoperatively and on postoperative day 1, 7(rst week), 30 (rst month), 90 (third month), and 180 (sixthmonth). �e mean thickness of the 1mm and 1–3mm ringswas calculated and used for further statistical analysis.

2.2. Statistical Analysis. �e IBM SPSS version 20.0 (IBMCorporation, Armonk, NY, USA) software was used forstatistical analyses. Measured data were described as the

Figure 1: Borders of automatically segmented retinal layers onOCT images. ILM, internal limiting membrane and inner border ofthe RNFL layer; RNFL, outer border of the retinal nerve ber layer;GCL, outer border of the ganglion cell layer; IPL, outer border ofthe inner plexiform layer; INL, outer border of the inner nuclearlayer; OPL, outer border of the outer nuclear layer; ELM, externallimiting membrane—outer border of the outer nuclear layer; RPE,retina pigment epithelium; BM, Bruch’s membrane.

800

700

600

500

Retin

a thi

ckne

ss (μ

m)

400

300

200

100

0

Figure 2: ETDRS grid for 1mm and 1–3mm circles on OCTimages. ETDRS grid on macula. C, central 1mm zone in macula;S, superior quadrant in 1–3mm circle onmacula; I, inferior quadrantin 1–3mm circle on macula; T, temporal quadrant in 1–3mm circleon macula; N, nasal quadrant in 1–3mm circle on macula.

2 Journal of Ophthalmology

arithmetic mean± standard deviation, whereas categoricaldata were described as percentages (%). Normal distributionof measured data was examined by the Kolmogorov–Smirnovtest. )e one-way ANOVA test was used for intergroupcomparison variables for repeated measures. )e Bonferronimethod was used to correct the p value. )e relationshipbetween EPT and TE and all thickness parameters were an-alyzed with the Pearson correlation analysis. A statistical levelof significance was accepted at p< 0.05.

3. Results

)emean age of the patients consisting of 25 (78%)males and7 (22%) females was 63.81± 9.0 years (range: 48–79 years).)ere were 20 right and 12 left eyes. )e mean preoperativeaxial length was 23.62± 0.9mm (range: 21.3–25.2mm). )ecataract type was nuclear sclerosis in 16 (50%) cases, posteriorsubcapsular in 12 (37.5%) cases, cortical in 3 (9.4%) cases, andcortical + posterior subcapsular in one (3.1%) case.

We found statistically significant differences in TRT andTRV in the 1mm circle and TRT, TRV, ONL, OPL, INL, IPLGCL, and NFL in the 1–3mm circle compared to the

preoperative values during the follow-up visits continuing for6 months (p< 0.05). )e study results showed a remarkabledecrease in TRT, TRV, and the thickness of most retinal layersat the first day visit after surgery. However, an increase wasthen observed in all parameters and reached approximately thepreoperative values at the first week visit.)e thickest TRTandretinal layer thickness values were observed at the first andthird month visits. A slight decrease, not reaching the pre-operative levels, was then seen in almost all parameters at thesixth month visit. We also noticed that the least affected layerswere the RPE and OPL. )e results are presented in Table 1.

)e mean effective phacoemulsification time and totalenergy were 62.46± 45.03 seconds and 6.41± 7.34, respectively.)ere was a positive correlation between EPTand TE and GCLin the 1mm circle and INL in the 1–3mm circle (p< 0.05 andTable 2).)ere was no significant correlation between EPTandTE and other retinal layers, TRT and TRV (p> 0.05).

4. Discussion

)emain triggering factor of PCME is thought to be surgicaltrauma of intraocular tissues by inducing the release of

Table 1: )ickness of macula TRT, TRV, and retinal layers with at the ETDRS circle of 1 and 3 millimeters.

Preoperative Postoperativeday 1Postoperative

week 1Postoperativemonth 1

Postoperativemonth 3

Postoperativemonth 6 p

TRT 1mm circle 276.63± 27.36 272.14± 26.12∗ 274.85± 26.74 279.81± 25.80 280.65± 26.82∗ 277.85± 26.22

inflammatory mediators although other possible mechanismssuch as photic retinopathy or vitreous traction have also beenimplicated [5]. Inflammatory mediators (prostaglandins,cytokines, and other vascular permeability factors) are knownto be released from the anterior segment of the eye aftersurgery and then diffuse into the vitreous cavity and retina,stimulating the breakdown of the blood-retinal barrier (BRB)and subsequent leakage of fluids across the retinal vessel walland into the perifoveal retinal tissues, resulting in macularedema [3]. )is edema usually resolves spontaneously andonly about 1–3% of cases persist, corresponding to clinicalPCME with persistent symptoms [6]. Although FFA used tobe considered the diagnostic gold standard for PCME, OCT isnow the method of choice, being a noninvasive technique forPCME evaluation and follow-up [3].

Optical coherence tomography is a useful device todetect intraretinal cysts that indicate clinical PCME and candecrease vision noninvasively after cataract surgery [3].Assessing the retinal layers in vivo may provide more in-formation to elucidate the pathologic processes involved insubclinical PCME. We therefore evaluated retinal layers byOCT after uncomplicated cataract surgery and presentedlong-term follow-up results on TRT, TRV, and retinal layerthickness according to the ETDRS grid. We noticed that theRPE and OPL were the least affected layers. In general, weobserved a decrease in TRT, TRV, and most retinal layers atthe first postoperative day visit. An increase was then seen inall thickness parameters and reached approximately thepreoperative levels at the first week visit.)e largest TRTandretinal layer thickness values were observed at the first andthird month visits. At the sixth month visit, a slight decreasewas seen in almost all parameters. However, this decreasedid not reach preoperative thickness levels. )ere wasa significant thickness increase in all retinal layers exceptRPE and OPL in the 1–3mm circle.

Grewing and Becker measured the retinal thicknessbefore and 0.5 hours after cataract surgery in 10 patients andreported a decrease that was not statistically significant [7].We noticed a decrease in TRT, TRV, and the thickness ofmost retinal layers after the first postoperative day. Perenteet al. [8] also reported a mild postoperative retinal thicknessthat was not statistically significant. According to the au-thors, the decrease observed in the first postoperative daymay be related to the previous light-scattering effect of thecataract that was possibly disrupting the optical quality ofthe OCTimaging [8]. However, there is not enough evidenceor information in the literature to fully explain the cause.

Šiško et al. [9] reported highest retinal thickness in theETDRS grid areas one month after uncomplicated cataractsurgery. )ey also stated mild decreasing trend in themeasurements from the first month to the sixth month,without reaching preoperative levels. Most studies havereported an increase in macular thickness after un-complicated cataract surgery [8, 10–16]. Gharbiya et al. [10]reported a significant macular thickness increase for up tosix postoperative months in 40 healthy patients. Falcão et al.[11] also found increased central macular thickness post-operatively and reported this as a nonpathological change.Cagini et al. [12] found an asymptomatic postoperative

macular thickness increase at 12 weeks in 62 eyes witha follow-up period of 28 weeks.)ese results are all similar toours. Gołebiewska et al. [17] reported increased retinalthickness and retinal volume during follow-up continuingfor 6 months after uncomplicated cataract surgery. Weobserved increased retinal volume after surgery, like others.

Measuring each retinal layer separately makes it easier tosee alteration in retinal structures than the TRT. It is unclearwhich retinal layer(s) has the most effect on increasing theretinal thickness. We found an increase in the thickness ofNFL, GCL, IPL, INL, and ONL and a decrease in OPL, butthese changes were only significant in the 1–3mm circle at thepostoperative sixth month follow-up when compared to thepreoperative measurements. RPE thicknesses were generallystable except for the first visit, but this first-visit change wasnot significant. We found increased GCL thickness in the1mm circle and INL thickness in the 1–3mm circle withmore TE and EPT. Another study reported a statisticallysignificant relationship between increased retinal thicknessand higher perioperative phaco power [17]. However, there isno study comparing postoperative retinal layer thickness withTE and EPT values.

)e INL includes the nuclei of the bipolar, horizontal,amacrine, and Muller cells. )e deep capillary plexus is alsoin this layer. Park et al. [18] have shown that the vascularendothelial growth factor (VEGF) has a crucial role in thevitality of the amacrine and bipolar cells. Sigler et al. [19]have reported cystic changes in the INL and ONL in patientswith clinical PCME. We did not find clinical PCME andtherefore did not observe cystic changes in any of our pa-tients; an increased thickness of the INL may be related tothe inflammatory effects of VEGF, which is an inflammatorymediator [20]. INL thickness was also increased in relationto optic neuritis, which is an inflammatory disease, in an-other study [21]. In the neurology literature, the use of INLas a parameter to monitor the efficacy of anti-inflammatorytreatments in multiple sclerosis has been proposed [22]. )esuperficial capillary plexus is located in the NFL, and itshyperpermability may have been responsible for the sig-nificantly increased thickness of the NFL and GCL in ourstudy.

Nepafenac (Alcon Research Ltd., Fort Worth, TX, USA),a topical ocular nonsteroidal anti-inflammatory drug(NSAID) used to treat the pain and inflammation associatedwith cataract surgery, is available as an ophthalmic sus-pension in concentrations of 0.1% and 0.3% [23]. Unlikeother NSAIDs, nepafenac is a prodrug that is deaminated toits active metabolite (amfenac) in the ocular tissues. It isa potent inhibitor of the cyclooxygenase (COX) isoformsCOX-1 and COX-2 and is distributed rapidly in both theanterior and posterior segments of the eye. It is well knownthat the retinal thickness increase is significantly lower inpatients administered an NSAID after cataract surgery [23, 24].It may therefore be better to avoid NSAID use when evaluatingretinal layer thickness after cataract surgery.

Our study has a few limitations. First, the sample sizecould be larger. Second, the retinal thickness values con-tinued to show a slight decrease at the sixth month visit, andthe follow-up should therefore be longer than 6 months.

4 Journal of Ophthalmology

In conclusion, we presented the six-month follow-upresults of TRT, TRV, and retinal layer thickness after un-complicated cataract surgery in this study.)e thickest valueswere observed at the first and third month visits. A slightdecrease without reaching preoperative levels was found in allthickness parameters at the sixth month visit. )e post-operative thickness increase was more prominent in the1–3mm circle than in the 1mm circle. On the other hand,OPL was the only retinal layer with decreased thickness aftersurgery. )ese findings may be useful for understanding thepathophysiological pathways of PCME. )e results suggestthat long-term follow-up of more than 6 months is neededto see whether total retinal and segmental changes return topreoperative levels.

Data Availability

)e data used to support the findings of this study areavailable from the corresponding author upon request.

Ethical Approval

All procedures performed in studies involving human par-ticipants were in accordance with the ethical standards of theinstitutional and/or national research committee and with the1964 Declaration of Helsinki and its later amendments orcomparable ethical standards.)is study was approved by theethics committee of Ankara Numune Training and ResearchHospital on 14.12.2016 and number 1113/2016.

Consent

Informed consent was obtained from all individual partic-ipants included in the study.

Disclosure

)e authors declare that the manuscript has not beenpublished previously nor under consideration for publica-tion elsewhere, in whole or in part.

Conflicts of Interest

)e authors declare that they have no conflicts of interest.

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