Ophthalmic Surgery, Lasers and Imaging Retina

Clinical Science 

Visualizing Macular Structures During Membrane Peeling Surgery With an Intraoperative Spectral-Domain Optical Coherence Tomography Device

Christoph Leisser, MD; Christoph Hackl, MD; Nino Hirnschall, MD, PhD; Nikolaus Luft, MD; Birgit Döller; Petra Draschl, MD; Karl Rigal, MD; Oliver Findl, MD, MBA

Abstract

BACKGROUND AND OBJECTIVE:

The aim of this study was to examine the quality of intraoperative visualization of the posterior hyaloid, epiretinal membrane (ERM), inner limiting membrane (ILM), and hyporeflective subfoveal zone with a commercially available, microscope-integrated spectral-domain OCT setup (mi-SD-OCT) (Rescan 700; Carl Zeiss Meditec AG, Germany).

PATIENTS AND METHODS:

Twenty patients prospectively scheduled for pars plana vitrectomy with membrane peeling due to an idiopathic ERM were included. Standard 23-gauge, three-port pars plana vitrectomy with membrane peeling and staining of the ERM with a trypan blue-based chromovitrectomy dye was performed in all cases. Intraoperative SD-OCT was performed before and after peeling and visualization of the posterior hyaloid, ERM, ILM, and presence of subfoveal hyporeflective zones were examined. OCT follow-ups were performed 2 days and 3 months after surgery. The study was approved by the local ethics committee of the city of Vienna.

RESULTS:

Successful intraoperative visualization of ERM by mi-SD-OCT was possible in all cases. The posterior hyaloid and ILM could not be seen in the mi-SD-OCT scans, whereas an intraoperative subfoveal hyporeflective zone presented in 35% of cases. In 12.5% an independent subfoveal hyporeflective zone presented postoperatively. Visual acuity improved in 93.8% of patients after surgery.

CONCLUSION:

mi-SD-OCT appears to be a valuable tool for intraoperative visualization of the ERM and offers immediate visualization of retinal anatomy during peeling. Therefore, it adds to the understanding of intraoperative traumatic changes due to the peeling procedure.

[Ophthalmic Surg Lasers Imaging Retina. 2016;47:328–332.]

Abstract

BACKGROUND AND OBJECTIVE:

The aim of this study was to examine the quality of intraoperative visualization of the posterior hyaloid, epiretinal membrane (ERM), inner limiting membrane (ILM), and hyporeflective subfoveal zone with a commercially available, microscope-integrated spectral-domain OCT setup (mi-SD-OCT) (Rescan 700; Carl Zeiss Meditec AG, Germany).

PATIENTS AND METHODS:

Twenty patients prospectively scheduled for pars plana vitrectomy with membrane peeling due to an idiopathic ERM were included. Standard 23-gauge, three-port pars plana vitrectomy with membrane peeling and staining of the ERM with a trypan blue-based chromovitrectomy dye was performed in all cases. Intraoperative SD-OCT was performed before and after peeling and visualization of the posterior hyaloid, ERM, ILM, and presence of subfoveal hyporeflective zones were examined. OCT follow-ups were performed 2 days and 3 months after surgery. The study was approved by the local ethics committee of the city of Vienna.

RESULTS:

Successful intraoperative visualization of ERM by mi-SD-OCT was possible in all cases. The posterior hyaloid and ILM could not be seen in the mi-SD-OCT scans, whereas an intraoperative subfoveal hyporeflective zone presented in 35% of cases. In 12.5% an independent subfoveal hyporeflective zone presented postoperatively. Visual acuity improved in 93.8% of patients after surgery.

CONCLUSION:

mi-SD-OCT appears to be a valuable tool for intraoperative visualization of the ERM and offers immediate visualization of retinal anatomy during peeling. Therefore, it adds to the understanding of intraoperative traumatic changes due to the peeling procedure.

[Ophthalmic Surg Lasers Imaging Retina. 2016;47:328–332.]

Introduction

Epiretinal membranes (ERMs) are disorders involving the posterior pole of the eyeball with loss of vision, especially in case of inner segment/outer segment junction disorders. Vitrectomy and membrane peeling are the gold standard for improvement of patients' vision and reduction of metamorphopsia by relieving tractional forces on retinal structures caused by the ERM.1 During the last decade, optical coherence tomography (OCT) became the leading diagnostic tool for macular diseases. Spectral-domain OCT (SD-OCT) is currently the most-developed and commercially available OCT setup, showing remarkable improvements in scanning speed and image resolution compared to the previous time-domain OCT. Pre- and postoperative imaging of retinal diseases enables detailed information of microstructures in the macula for planning the surgical procedure.2

Intraoperative use of OCT is a new technological improvement to aid intraoperative imaging and documentation during the procedure. Different study groups have already presented intraoperative SD-OCT setups3–16 and even work with operating microscope-integrated SD-OCT setups.5–11,16

The aim of our study was to examine the quality of intraoperative visualization of the posterior hyaloid, ERM, inner limiting membrane (ILM), and hyporeflective subfoveal zone with a commercially available, continuous intraoperative microscope-integrated SD-OCT setup (mi-SD-OCT) (Rescan 700; Zeiss, Oberkochen, Germany).

Patients and Methods

This prospective, interventional, single-center study included patients scheduled for pars plana vitrectomy with membrane peeling due to ERM with or without a lamellar hole of the macula. Inclusion criteria were an age older than 21 years and no co-morbidities, such as diabetes mellitus, glaucoma, retinopathia pigmentosa, or any form of age-related macular degeneration. All the research and measurements followed the tenets of the Declaration of Helsinki and were approved by the local ethics committee of the city of Vienna ( ClinicalTrials.gov identifier: NCT02319655). Written informed consent was obtained from all patients in the study.

Surgery was performed as standard, including 23-gauge, three-port pars plana vitrectomy and membrane peeling. Three experienced vitreoretinal surgeons participated in the study (OF, CL, KR). To visualize the ERM and ILM, chromovitrectomy with a trypan blue-based dye (Membrane Blue Dual; DORC, the Netherlands) was performed. Additionally, mi-SD-OCT scans were performed at several different time points: at the beginning of surgery (before induction of a posterior hyaloid detachment) and after the posterior hyaloid was fully detached from the macula. A third scan was acquired after the surgeon had decided that ERM peeling was completed. If needed, additional peeling to remove ERM remnants or the ILM, visualized by mi-SD-OCT and repeated staining, was performed and a further mi-SD-OCT scan was taken. Just before, 2 days, and 3 months after surgery, macular OCT scans were performed with a comparable commercially available standalone SD-OCT (Cirrus HD-OCT, Carl Zeiss Meditec, Dublin, CA). As the mi-SD-OCT consists of the same OCT setup as the SD-OCT for pre- and postoperative examinations, comparability of the results was ensured. Two examiners (CH, CL) independently reviewed the generated mi-SD-OCT videos and 3-D cubes independently from each other. For intraobserver reproducibility, one examiner (CL) reviewed all mi-SD-OCT videos 4 weeks after baseline reviewing of the videos. Therefore, all videos were anonymized and shown in a randomized fashion to reduce recognition bias. Best-corrected distance visual acuity was performed with EDTRS charts preoperatively and at 3 months postoperatively.

Statistical Analysis

For statistical analysis, Microsoft Excel 2011 for Mac (Microsoft, Redmond, WA) with a StatPlus:mac version 5.8.3.8 plug-in (AnalystSoft, Walnut, CA) and a XLSTAT 2012 plug-in (Addinsoft, New York, NY) were used. For missing data, observations were excluded from analysis.

Results

In total, 20 eyes of 20 patients were included. Median age was 70 years (range: 57 years to 88 years) and the female-to-male distribution was 12:8. The number of left and right eyes was equally distributed (10:10). In five eyes, an additional lamellar hole of the macula was detected prior to surgery.

Successful intraoperative visualization of the ERM was possible in all cases at the beginning of surgery (Figures 13). Inter- and intraobserver reproducibility was found to be 100% for ERM detection at this time point. Mi-SD-OCT scanning after ERM peeling showed ERM remnants in 40% of cases, which occurred in 5% (one case) in the foveal region and in 35% (seven cases) in the perifoveal region. In five of these cases, the findings of the mi-SD-OCT lead to an additional peeling of the foveal/perifoveal ERM to reduce traction on the fovea. Inter- and intraobserver reproducibility was found to be 94.7% at this time point. Restaining was performed before an additional peeling in all cases due to the study protocol and could confirm the presence of ERM remnants in all six cases. It also offered additional enhancement of edges of ERM remnants compared to mi-SD-OCT, as well as enabled easier peeling.


Subfoveal hyporeflective zone, occurring during the peeling procedure, due to traction (the peeled portion of the epiretinal membrane is marked with arrow 1 and the subfoveal hyporeflective zone with arrow 2).

Figure 1.

Subfoveal hyporeflective zone, occurring during the peeling procedure, due to traction (the peeled portion of the epiretinal membrane is marked with arrow 1 and the subfoveal hyporeflective zone with arrow 2).


The subfoveal hyporeflective zone shown in Figure 1 decreases during the further peeling procedure.

Figure 2.

The subfoveal hyporeflective zone shown in Figure 1 decreases during the further peeling procedure.


With increasing distance to the peeled portion of the epiretinal membrane, the subfoveal hyporeflective zone shown in Figure 1 disappears.

Figure 3.

With increasing distance to the peeled portion of the epiretinal membrane, the subfoveal hyporeflective zone shown in Figure 1 disappears.

Intraoperative visualization of the attached hyaloid with the mi-SD-OCT was not successful in any of the cases. Preoperative SD-OCT scanning detected an attached hyaloid in 10% (two cases) and intraoperative funduscopic findings detected an attached hyaloid in five more cases for a total of 35% (seven cases), altogether.

Intraoperative visualization of the ILM with the mi-SD-OCT at any stage of the peeling surgery was not possible in any of our patients.

The occurrence of an intraoperative subfoveal hyporeflective zone in the mi-SD-OCT was found in 30% (six cases) with an inter- and intraobserver reproducibility of 94.7% (Figure 1). In one of these cases, the subfoveal hyporeflective zone was also detectable in the postoperative SD-OCT scans, but in all other cases it had already disappeared by that time point. Two patients presented a subfoveal hyporeflective zone 2 to 3 days after surgery without having had intraoperative hyporeflective zones during surgery. These were resorbed at least 4 days later.

Best-corrected distance visual acuity improved in 15 patients and decreased in one patient 3 months after surgery. Four patients were lost to follow-up after surgery.

Discussion

mi-SD-OCT displays a new application of OCT technology in ophthalmology.5–11,16 Due to the good transparency of ocular media and the technical improvements in OCT-technology, OCT plays a leading role among the diagnostic tools in ophthalmology. The investigated commercially available mi-SD-OCT showed an excellent inter- and intraobserver reproducibility for ERM visualization at different operative time points. The ERM could be visualized by mi-SD-OCT in all of our patients, contributing to immediate visualization of iatrogenic-induced changes in retinal pathology during the peeling. The decision for enlarging the peeled zone (in our study population, 20%) could be indicated out of the mi-SD-OCT scans. Restaining confirmed that information and additionally enhanced visualization of edges of the ERM-remnants for easier peeling.

Image quality in mi-SD-OCT did not reach the quality of the standalone SD-OCT. However, inter- and intraobserver reproducibility was excellent, even for structures that were difficult to detect, such as the subfoveal hyporeflective zone or ERM remnants. Possible reasons for decreased image quality in the mi-SD-OCT could be an intraoperative epithelial edema of the cornea and the fact that OCT passes the optical pathway of the operating microscope. Reports of Ehlers et al.12,13 about enhanced visualization in intraoperative OCT with indocyanine green or triamcinolone acetonide show a possible way to overcome that limitation, but we believe the main potential of mi-SD-OCT lies in the possibility of immediate visualization of iatrogenic surgery induced changes in the retinal structure, peeling without use of a dye and adapting the peeling strategy according to the traction seen on the retina. Falkner-Radler et al. reported a peeling rate without dye in 40% of their patients.16

We could not visualize the posterior hyaloid and ILM in a reproducible manner, showing fields for improvement in the next generations of the used mi-SD-OCT setup, as vitreomacular traction syndrome is principally visible in intraoperative OCT.3,17 For peeling the ILM, chromovitrectomy is still recommended to ensure complete and safe ILM-peeling.

Subfoveal hyporeflective zones during ERM peeling14,15 resemble a remarkable detail of peeling surgery, present in six (30%) of our patients. Figure 1 presents a hyporeflective zone in the moment of traction due to the peeling procedure. In that case, the tractive component of the subfoveal hyporeflective zone immediately disappeared after the traction was resolved (Figure 3). These could be seen in the postoperative SD-OCT examinations of only one of our six patients with intraoperative subfoveal hyporeflective zones. These six cases present intraoperative traction as one of the possible reasons for an intraoperative and/or postoperative subfoveal hyporeflective zone. Postoperative subfoveal hyporeflective zones without documented presence of traction-induced intraoperative subfoveal hyporeflective zones presented in two patients. The impact of subfoveal hyporeflective zones on postoperative visual rehabilitation will need to be examined in larger studies.

In conclusion, in all cases where membrane peeling due to ERM was indicated, mi-SD-OCT was a valuable tool for improving surgical results, despite decreased image quality compared to pre- or postoperative SD-OCT. Furthermore, mi-SD-OCT gives additional understanding of iatrogenic changes of retinal pathology, such as intraoperative traction-induced subfoveal hyporeflective zones.

References

  1. Machemer R. The surgical removal of epiretinal macular membranes (macular puckers). Klin Monbl Augenheilkd. 1978;173(1):36–42.
  2. Shimozono M, Oishi A, Hata M, et al. The significance of cone outer segment tips as prognostic factor in epiretinal membrane surgery. Am J Ophthalmol. 2012;153(4):698–704. doi:10.1016/j.ajo.2011.09.011 [CrossRef]
  3. Dayani PN, Maldonado R, Farsiu S, Toth CA. Intraoperative use of handheld spectral domain optical coherence tomography imaging in macular surgery. Retina. 2009;29(10):1457–1468. doi:10.1097/IAE.0b013e3181b266bc [CrossRef]
  4. Joos KM, Shen JH. Miniature real-time intraoperative forward-imaging optical coherence tomography probe. Biomed Opt Express. 2013;4(8):1342–1250. doi:10.1364/BOE.4.001342 [CrossRef]
  5. Tao YK, Ehlers JP, Toth CA, Izatt JA. Intraoperative spectral domain optical coherence tomography for vitreoretinal surgery. Opt Lett. 2010;35(20):3315–3317. doi:10.1364/OL.35.003315 [CrossRef]
  6. Binder S, Falkner-Radler CI, Hauger C, Matz H, Glittenberg C. Feasibility of intrasurgical spectral-domain optical coherence tomography. Retina. 2011;31(7):1332–1336. doi:10.1097/IAE.0b013e3182019c18 [CrossRef]
  7. Ehlers JP, Tao YK, Farsiu S, Maldonado R, Izatt JA, Toth CA. Integration of a spectral domain optical coherence tomography system into a surgical microscope for intraoperative imaging. Invest Ophthalmol Vis Sci. 2011;528(6):3153–3159. doi:10.1167/iovs.10-6720 [CrossRef]
  8. Hahn P, Migacz J, O'Connell R, Izatt JA, Toth CA. Unprocessed real-time imaging of vitreoretinal surgical maneuvers using a microscope-integrated spectral-domain optical coherence tomography system. Graefes Arch Clin Exp Ophthalmol. 2013;251(1):213–220. doi:10.1007/s00417-012-2052-2 [CrossRef]
  9. Hahn P, Migacz J, O'Donnell R, et al. Preclinical evaluation and intraoperative human retinal imaging with a high-resolution microscope-integrated spectral domain optical coherence tomography device. Retina. 2013;33(7):1328–1337. doi:10.1097/IAE.0b013e3182831293 [CrossRef]
  10. Ehlers JP, Kaiser PK, Srivastava SK. Intraoperative optical coherence tomography using the Rescan 700: preliminary results from the DISCOVER study. Br J Ophthalmol.2014;98(10):1329–1332. doi:10.1136/bjophthalmol-2014-305294 [CrossRef]
  11. Ehlers JP, Srivastava SK, Feiler D, Noonan AI, Rollins AM, Tao YK. Integrative advances for OCT-guided ophthalmic surgery and intraoperative OCT: microscope integration, surgical instrumentation, and heads-up display surgeon feadback. PLoS One. 2014;9(8):e105224. doi:10.1371/journal.pone.0105224 [CrossRef]
  12. Ehlers JP, McNutt S, Kaiser PK, Srivastava SK. Contrast-enhanced intraoperative optical coherence tomography. Br J Ophthalmol. 2013;97(11):1384–1386. doi:10.1136/bjophthalmol-2012-303048 [CrossRef]
  13. Ehlers JP, McNutt S, Dar S, Tao YK, Srivastava SK. Visualisation of contrast-enhanced intraoperative optical coherence tomography with indocyanine green. Br J Ophthalmol. 2014;97(11):1588–1591. doi:10.1136/bjophthalmol-2014-305295 [CrossRef]
  14. Ray R, Baranano DE, Fortun JA, et al. Intraoperative microscope-mounted spectral domain optical coherence tomography for evaluation of retinal anatomy during macular surgery. Ophthalmology. 2011;118(11):2212–2217. doi:10.1016/j.ophtha.2011.04.012 [CrossRef]
  15. Pichi F, Alkabes M, Nucci P, Ciardella AP. Intraoperative SD-OCT in macular surgery. Ophthalmic Surg Lasers Imaging. 2012;43(6 Suppl):S54–60. doi:10.3928/15428877-20121001-08 [CrossRef]
  16. Falkner-Radler CI, Glittenberg C, Gabriel M, Binder S. Intrasurgical microscope-integrated spectral domain optical coherence tomography-assisted membrane peeling. Retina. 2015;35(10):2100–2106. doi:10.1097/IAE.0000000000000596 [CrossRef]
  17. Ehlers JP, Tam T, Kaiser PK, Martin DF, Smith GM, Srivastava SK. Utility of intraoperative optical coherence tomography during vitrectomy surgery for vitreomacular traction syndrome. Retina. 2014;34(7):1341–1346. doi:10.1097/IAE.0000000000000123 [CrossRef]
Authors

From the Vienna Institute for Research in Ocular Surgery, a Karl Landsteiner Institute, Hanusch Hospital, Vienna, Austria (LC, HC, HN, LN, DB, DP, RK, FO); and the Moorfields Eye Hospital NHS Foundation Trust, London, UK (FO).

Previously presented in part at the Second Intraoperative OCT Science Day on February 21, 2015, in Vienna, Austria.

Dr. Findl is a scientific advisor for Carl Zeiss Meditec AG. The remaining authors report no relevant financial disclosures.

Address correspondence to Oliver Findl, MD, MBA, Hanusch Hospital, Heinrich-Collin-Strasse 30, 1140-Vienna, Austria; 43-1-91021-84611; fax: 43-1-91021-84619; email: oliver@findl.at.

Received: November 24, 2015
Accepted: February 19, 2016

10.3928/23258160-20160324-04

Sign up to receive

Journal E-contents