Intraoperative SD-OCT in Macular Surgery

S54 COPYRIGHT © SLACK INCORPORATED

■ C L I N I C A L S C I E N C E ■

INTRODUCTION

Imaging technology of macular pathology has improved significantly over the past decade. Spectral-

domain optical coherence tomography (SD-OCT), the latest generation of OCT, offers several advantag-es over time-domain OCT. SD-OCT enables physi-cians to noninvasively obtain detailed retinal images

From San Giuseppe Hospital (FP, MA, PN), University Eye Clinic, Milan; and Policlinico Sant’Orsola-Malpighi (APC), Ophthalmology Unit, Bologna, Italy.

Originally submitted May 14, 2012. Accepted for publication October 1, 2012.

The authors have no financial or proprietary interest in the materials presented herein.

Address correspondence to Francesco Pichi, MD, San Giuseppe Hospital, University Eye Clinic, Via San Vittore, 12, 20123 Milan, Italy. E-mail: ilmiticopicchio@

gmail.com

doi: 10.3928/15428877-20121001-08

n BACKGROUND AND OBJECTIVE: Intraoper-ative use of spectral-domain optical coherence tomog-raphy (SD-OCT) using an OCT-mounted surgical microscope could provide additional information to predict visual outcomes of macular surgery and identi-fy intraoperative changes in the macular anatomy that affect visual recovery.

n PATIENTS AND METHODS: This intervention-al retrospective case study included 5 eyes of 5 con-secutive patients with various macular pathologies. All patients underwent the standard surgery for idiopathic macular holes and epiretinal membranes (ERMs) us-ing the same 25-gauge three-port pars plana technique. If present, the ERM was removed. The dye procedure was then repeated to stain and remove the internal lim-iting membrane (ILM). OCT images were obtained with the retinal map or cross-section program preinci-sion, post-hyaloid elevation (if applicable), post-residu-al ERM peel (if applicable), and post-ILM peel.

n RESULTS: In 3 of 5 patients, the intraoperative scan revealed an increased area of subretinal hypore-flectivity corresponding with a clinically visible “cuff ” of retinal detachment. In 2 patients, the SD-OCT scan taken immediately after ERM removal helped find a cleavage plane for the subsequent ILM peeling, which could be further confirmed by a scan taken immedi-ately after it. In 2 cases, the scans identified intraopera-tive complications that otherwise would not have been noted and allowed the surgeon to modify the next pro-cedures during surgery.

n CONCLUSION: Use of this technology in an operative setting can provide greater insight into the changes in retinal anatomy created during macular surgery.

[Ophthalmic Surg Lasers Imaging 2012;43:S54-S60.]

Intraoperative SD-OCT in Macular Surgery

Francesco Pichi, MD; Micol Alkabes, MD; Paolo Nucci, MD; Antonio P. Ciardella, MD

OPHTHALMIC SURGERY, LASERS & IMAGING · VOL. 43, NO. 6 (SUPPL), 2012 S55

of various retinal diseases in a clinical environment.1-4 Ultrastructural details of the inner segment/outer seg-ment (IS/OS) junction of the photoreceptor layer can be appreciated and anatomic changes in this layer be-fore and after macular surgery have been correlated with visual outcomes.5-10 This higher resolution of SD-OCT has also provided more information about the hyaloid–retinal interface. SD-OCT reveals a more complete understanding of vitreomacular traction and epiretinal membrane (ERM) and their overlap in morphology.11-13

Intraoperative use of SD-OCT using an OCT-mounted surgical microscope or a handheld SD-OCT device has been attractive because OCT images can be obtained immediately during vitreoretinal surger-ies and used to detect retinal ultrastructural changes resulting from the surgical procedures, as well as to de-cide on the next procedures to be taken during surgery. Intraoperative SD-OCT imaging of the macula could provide additional information to predict visual out-comes and identify changes in the macular anatomy occurring during surgery that affect visual recovery. This article describes intraoperative changes to retinal anatomy during macular surgery and compares intra-operative findings with postoperative results.

PATIENTS AND METHODS

PatientsThis interventional retrospective case study in-

cluded 5 eyes of 5 consecutive patients with various macular pathologies (1 vitreomacular traction syn-drome, 2 ERMs, and 2 full-thickness macular holes). All patients were naive to treatment for idiopathic macular holes and ERM and underwent the primary surgery at Sant’Orsola-Malpighi Hospital, Bologna, Italy. All five patients underwent a complete preoper-ative ophthalmic examination, including dilated fun-dus examination using an indirect ophthalmoscope and 90+ diopter noncontact lens slit-lamp biomicros-copy. In addition to routine ophthalmic examination, SD-OCT foveal scan and retinal mapping (Spectralis HRA+OCT; Heidelberg Engineering, Heidelberg, Germany) was performed preoperatively on all pa-tients. All patients were pseudophakic. The patients were followed up at 7 to 10 days and at 1 month after surgery with visual acuity examinations and using the same SD-OCT instrument.

Surgical ProcedureAll patients underwent the standard surgery for

idiopathic macular holes and ERMs by a single sur-geon (APC). Surgery was performed using the same 25-gauge three-port pars plana technique. The infu-sion was stopped with a stopcock, and 0.1 mL AQ:3 of Brilliant Peel (Fluoron Inc., Geuder, Germany) was injected over the retinal surface using an insulin syringe and blunt-tipped needle. After 30 seconds, the infu-sion was opened and the dye removed with passive ef-flux using an extrusion cannula. If present, the ERM was removed. The dye procedure was then repeated in every patient to stain and remove the internal limiting membrane (ILM). Eckardt ILM forceps (Dutch Oph-thalmic, Exeter, PA) were used in all cases to remove the ERM and/or ILM. A fluid–air exchange was per-formed for macular hole.

All patients were asked to lie in a prone position for several hours immediately after the surgery, after which they were allowed to take any position other than the supine position for 1 week.

OCT ExaminationsA handheld SD-OCT device (iVue-100; Optovue

Inc., Fremont, CA) was attached to a specially made OCT holder and used intraoperatively. The OCT im-ages of all eyes were obtained with the retinal map pro-gram or the cross-section program preincision, post-hyaloid elevation (if applicable), post-residual ERM peel (if applicable), and post-ILM peel. Images were analyzed for qualitative features. Anatomic landmarks were used to identify the same image slice at each time point. Qualitative measures such as foveal contour and the appearance of corrugations on the retinal surface were compared among the images at different time points. Instrument gauge, method of hyaloid elevation, type of stains used, and surgical results were recorded for all patients.

RESULTS

Case 1An 86-year-old man was referred to our clinic

for decreased visual acuity (VA) in the left eye. Best-corrected VA was 20/100, and vitreomacular traction syndrome with a thin ERM was noted on SD-OCT. Macular surgery was planned after the patient signed the informed consent. During surgery, a first SD-


OCT scan (Figure 1A) was taken to document the presence of the vitreomacular traction before starting the vitrectomy. A second OCT scan (Figure 1B) was performed after the removal of the ERM and vitreo-macular traction, revealing a small foveal detachment with elevation of the band corresponding to the IS/OS junction. Moreover, intraretinal cystic spaces were observed in the inner layers on intraoperative cross-sectional scan.

At 10 days postoperatively, his best-corrected VA was 20/60 and SD-OCT (Figure 1C) did not docu-ment any sign of elevation of the IS/OS layer, as seen intraoperatively, but revealed some residual cystic changes in the inner nuclear layer. Based only on this

postoperative scan, it could be thought that the mem-brane was successfully peeled and trauma only induced at the level of the inner retinal layers. However, the in-traoperative SD-OCT clearly shows that some of the forces of the ERM peel have transferred through the retina, at least to the level of the IS/OS and retinal pig-ment epithelium.

Case 2A 72-year-old woman with an ERM and a lamel-

lar macular hole (Figure 2A) in her right eye presented with a visual acuity of 20/100 and metamorphopsia. After the informed consent was signed, the patient un-derwent pars plana vitrectomy and peeling of the ERM.

Figure 1. (A) An intraoperative scan

through the fovea showing vitreo-

macular traction syndrome with a

table-top appearance. (B) After peel-

ing of the epiretinal membrane, some

cystic spaces in the inner retinal lay-

ers appear, along with a subfoveal

hyporeflective area consistent with a

shallow retinal detachment. (C) At 10

days postoperatively, the detachment

disappears but the cystic changes

are still present.

Figure 2. (A) A lamellar macular hole

visible on the optical coherence to-

mography scan, along with an epiret-

inal membrane. (B) After peeling of

the epiretinal membrane, the intraop-

erative scan shows the presence of

another membrane, probably the in-

ternal limiting membrane, which was

successfully peeled. (C) At 1 month

postoperatively, the retinal anatomy

is completely restored.


Figure 2B shows an intraoperative SD-OCT scan tak-en after the peeling of the ERM: a slightly hyperreflec-tive membrane was seen on the scan, temporally to the hole, and it was interpreted as the ILM, elevated after the overhanging ERM peeling. ILM peeling was there-fore performed, after staining with Brilliant Blue G. A tuft of vitreous could be seen adherent to the border of the lamellar hole.

One month postoperatively, B-scan revealed a res-olution of the lamellar hole (Figure 2C) and the best-corrected VA was 20/30.

Case 3A 77-year-old woman came to our attention com-

plaining of metamorphopsia in her right eye, with a best-corrected VA of 20/60. An SD-OCT (Figure 3A) scan showed a foveal pseudocyst with an ERM. The benefits and risks of surgery were explained to the pa-tient, and she agreed to undergo a pars plana vitrec-tomy and ERM peeling. An intraoperative scan (Figure 3B) was taken after peeling of the ERM, and it showed an iatrogenic full-thickness macular hole secondary to the mechanical traction forces of the peeling. The surgical plan was therefore modified, ILM peeling was performed, and intraocular gas (SF

6) was applied to

close the hole.Despite this complication, which the surgeon was

able to identify only with the intraoperative device, a 1-month postoperative scan revealed complete restora-tion of the retinal anatomy and best-corrected VA im-proved to 20/30.

Case 4A 71-year-old woman was diagnosed as having a

macular hole in the right eye 2 years previously, with a best-corrected VA of 20/80. The patient did not attend the following three visits scheduled, and when she was next seen, her visual acuity had deteriorated to 20/200 and the OCT scan showed a stage 4 full-thickness mac-ular hole (Figure 4A). The rare eventuality of visual im-provement after surgery was explained to the patient, but, despite that, she decided to undergo vitreoretinal surgery. An intraoperative scan was taken (Figure 4B) after pars plana vitrectomy and ILM peeling and it pointed out a rolled up nasal ILM remnant, a cuff of subretinal fluid with a diffuse hyporeflectivity between the retinal pigment epithelium and the neurosensory retina, and vitreous tufts still attached at the edges of the hole.

At 7 days postoperatively, the hole was com-pletely closed on OCT, but the ELM and the IS/OS junction were completely absent under the fovea and the inner retinal layers were atrophic due to the long-standing nature of the hole. Final best-corrected VA was 20/100.

Case 5A 61-year-old woman with diabetes mellitus pre-

sented with a stage 4 full-thickness macular hole in the right eye, which had been diagnosed 2 years previously, and best-corrected VA was 20/200. An SD-OCT scan confirmed the diagnosis (Figure 5A), and pars plana vitrectomy was planned. During surgery, an SD-OCT

Figure 3. (A) A foveal pseudocyst

due to an epiretinal membrane, treat-

ed with a peeling of the same. (B)

The intraoperative scan shows the

appearance of a full-thickness macu-

lar hole secondary to the tractional

forces of the peeling. (C) This compli-

cation, treated with gas tamponade,

did not prevent the complete restora-

tion of the foveal anatomy.


scan was taken right after the ILM peeling and revealed an extensive detachment of the neuroretinal layers from the underlying retinal pigment epithelium (Figure 5B). However, the surgical plan was not altered and SF

6 gas

was placed inside the eye.At 1 month postoperatively, the hole was com-

pletely closed, but the best-corrected VA remained as low as 20/100, mainly due to the complete absence on OCT of the outer hyperreflective bands. This anatomi-cal change could be due to the traumatic detachment induced by forceps during the ILM peeling; however, it seems more probable that the longstanding nature of the hole and the concomitant diabetic changes were the main causes of the poor VA recovery.

DISCUSSION

Many studies have described the clinical applica-tion of OCT and how it has revolutionized vitreoreti-nal practice. SD-OCT has provided greater resolution of retinal anatomy and visualized previously unknown pathologic changes that are correlated to visual prog-nosis.5-10,14,15 Use of this technology in an operative setting can provide greater insight into the changes in retinal anatomy created during macular surgery.16

Evaluation of the base of the macular hole during surgery revealed an increased area of subretinal hypo-reflectivity, which corresponds with the clinically vis-ible “cuff ” of subretinal fluid. We believe that this in-

Figure 4. (A) A stage 4 macular hole.

(B) The intraoperative scan, taken af-

ter the peeling of the internal limiting

membrane, shows a remnant of the

membrane rolled up nasally (B1), a

subretinal accumulation of fluid (B2),

and tufts of vitreous at the edges of

the hole (B3). (C) At 7 days postop-

eratively, the hole was closed.

Figure 5. (A) An intraoperative scan

taken before posterior hyaloid eleva-

tion shows a stage 4 macular hole.

(B) After internal limiting membrane

peeling, an iatrogenic retinal detach-

ment is revealed by the optical co-

herence tomography, extending both

nasally and temporally to the hole.

(C) Despite this complication, the

hole appeared completely closed at

1 month postoperatively.


crease in the area of subretinal hyporeflectivity might be due to the creation of a shallow retinal detachment. Whether the area or volume of this increased foveal de-tachment affects visual outcome requires further study. Herbert et al.17 evaluated subretinal fluid specimens obtained at the time of macular hole surgery. They dis-covered photoreceptors and macrophages in the milieu in a substantial number of patients. Whether these ele-ments were present owing to the pathologic process or to surgical manipulation is still not known. Our find-ings of increased foveal detachment during membrane manipulation, although acute and temporary, could lead to a loss of photoreceptors that could eventually influence functional outcomes.

All holes had IS/OS disruption in the perifoveal area preoperatively caused by a centrifugal dislocation of the retinal layers from tangential forces. This anom-aly did not get worse with peeling and seemed more related to the areas of foveal edema and not to areas of detachment caused by surgical manipulation.

It is well known that forces between the retina and vitreous body are transmitted via the ILM and that, for this reason, this membrane seems to play a great role in the pathogenesis of full-thickness macular holes. Thinking of the ILM as a scaffold for cellular prolifera-tion on which glial cells may migrate and thus create further tangential contractile force, ILM peeling has been widely accepted as an effective treatment option to achieve anatomic macular hole closure and func-tional recovery.18 Several studies have been published in the literature to assess the value of ILM peeling in macular hole surgery for its potential anatomical and visual success. Thus, the possibility to document its re-moval intraoperatively with OCT could improve the anatomical and functional outcome, especially in stage 3 and 4 macular holes. An SD-OCT scan taken imme-diately after ERM removal could help find a cleavage plane for the subsequent ILM peeling, which could be further confirmed by a scan taken immediately after it.

Manipulation with surgical instrumentation and ILM removal have been documented to cause damage to the nerve fiber layer, manifesting as dissociated op-tic nerve fiber layer,19 concentric macular dark spots,20 swelling of arcuate nerve fiber later,21 or paracentral scotoma.22 The tomographic intraoperative finding of increased subretinal fluid after ILM peeling could provide another possible mechanism to explain these changes.

The anatomy of the retinal surface changed in all patients after ERM peel. A corrugated appearance of the retinal surface was present after removal of the ILM.19,20 Improvement in retinal contour could be difficult to appreciate intraoperatively after the peel, but all patients showed improved surface contour in the postoperative period. A majority of patients had a disruption in the IS/OS junction that, as shown in previous studies,14,15 likely limits final vision. As with patients with macular hole, patients treated for ERM had IS/OS junction disruption that was perifoveal and related to areas of edema, and this disruption did not spread to areas of detachment after the peel.

Residual ERM and the edge of the ILM could be seen easily on SD-OCT and staining with Brilliant Peel accentuated edges of membrane on SD-OCT, which can be especially helpful at identifying the edge of the peel when the membrane edge is not up. This accen-tuation of tissue interfaces has been noted using other contrast agents with OCT.23

Similar to the patients undergoing vitrectomy for macular hole, the majority of our patients who under-went surgery for ERM developed new subretinal hypo-reflectance. As with the macular hole cases, this could represent a shallow neurosensory detachment of the retina. Another explanation for this could be stretching of the outer segments, leading to decreased reflectance. In these cases, routine manipulation by peeling the membrane may lead to a larger detachment by height and area.

In our series, the macular hole was closed in each case and all eyes that underwent ERM surgery had im-proved visual acuity and retinal anatomy at last follow-up. It would be interesting to evaluate intraoperative SD-OCT images of eyes that subsequently had worse outcomes. Although chronicity of pathology is among the greatest factors to determine prognosis, it is pos-sible that intraoperative changes, such as the increased subretinal fluid, may play a role as a consequence of some stretching forces exerted on the retinal layer.

This study is limited by the subjective nature of some findings. A prospective study with a larger sample of patients comparing preoperative, intraoperative, and postoperative SD-OCT findings and measurements would provide valuable information about how out-comes may be related to anatomic changes during sur-gery. Another major limitation of the use of OCT in an intraoperative setting is its inability to use an eye track-


ing system to scan the same region at different times; furthermore, in our case series two different devices were used to take the OCT scans preoperatively, in-traoperatively, and postoperatively, which could repre-sent a possible bias had we taken quantitative measure-ments, which we did not. Despite these limitations, integration of SD-OCT into the operating microscope and expanded use of the device will provide additional information about the anatomy of macular disease and its response to surgical treatment.

REFERENCES

1. Binder S, Falkner-Radler CI, Hauger C, Matz H, Glittenberg C. Fea-sibility of intrasurgical spectral-domain optical coherence tomogra-phy. Retina. 2011;31:1332-1336.

2. Dayani PN, Maldonado R, Farsiu S, Toth CA. Intraoperative use of handheld spectral domain optical coherence tomography imaging in macular surgery. Retina. 2009;29:1457-1468.

3. Wykoff CC, Berrocal AM, Schefler AC, Uhlhorn SR, Ruggeri M, Hess D. Intraoperative OCT of a full thickness macular hole before and after internal limiting membrane peeling. Ophthalmic Surg Lasers Imaging. 2010;41:7-11.

4. Chavala SH, Farsiu S, Maldonado R, Wallace DK, Freedman SF, Toth CA. Insights into advanced retinopathy of prematurity using hand-held spectral domain optical coherence tomography imaging. Oph-thalmology. 2009;116:2448-2456.

5. Sano M, Shimoda Y, Hashimoto H, Kishi S. Restored photoreceptor outer segment and visual recovery after macular hole closure. Am J Ophthalmol. 2009;147:313-318.

6. Oh J, Smiddy WE, Flynn HW Jr, et al. Photoreceptor inner/outer seg-ment defect imaging by spectral domain OCT and visual prognosis after macular hole surgery. Invest Ophthalmol Vis Sci. 2010;51:1651-1658.

7. Chalam KV, Murthy RK, Gupta SK, et al. Foveal structure defined by spectral domain optical coherence tomography correlates with visual function after macular hole surgery. Eur J Ophthalmol. 2010;20:572-527.

8. Inoue M, Watanabe Y, Arakawa A, et al. Spectral-domain optical coherence tomography images of inner/outer segment junctions and macular hole surgery outcomes. Graefes Arch Clin Exp Ophthalmol. 2009;247:325-330.

9. Chang LK, Koizumi H, Spaide RF. Disruption of the photorecep-tor inner segment-outer segment junction in eyes with macular holes. Retina. 2008;28:969-975.

10. Baba T, Yamamoto S, Arai M, et al. Correlation of visual recovery and presence of photoreceptor inner/outer segment junction in op-tical coherence images after successful macular hole repair. Retina. 2008;28:453-458.

11. Chang LK, Fine HF, Spaide RF, et al. Ultrastructural correlation of spectral-domain optical coherence tomographic findings in vitreo-macular traction syndrome. Am J Ophthalmol. 2008;146:121-127.

12. Koizumi H, Spaide RF, Fisher YL, et al. Three-dimensional evalu-ation of vitreomacular traction and epiretinal membrane using spectral-domain optical coherence tomography. Am J Ophthalmol. 2008;145:509-517.

13. Legarreta JE, Gregori G, Knighton RW, et al. Three dimensional spec-tral-domain optical coherence tomography images of the retina in the presence of epiretinal membranes. Am J Ophthalmol. 2008;145:1023-1030.

14. Arichika S, Hangai M, Yoshimura N. Correlation between thickening of the inner and outer retina and visual acuity in patients with epireti-nal membrane. Retina. 2010;30:503-508.

15. Falkner-Radler CI, Glittenberg C, Hagen S, et al. Spectral-domain optical coherence tomography for monitoring epiretinal membrane surgery. Ophthalmology. 2010;117:798-805.

16. Dayani PN, Maldonado R, Farsiu S, Toth CA. Intraoperative use of handheld spectral domain optical coherence tomography imaging in macular surgery. Retina. 2009;29:1457-1468.

17. Herbert EN, Sheth HG, Wickremasinghe S, et al. Nature of subreti-nal fluid in patients undergoing vitrectomy for macular hole: a cyto-pathological and optical coherence tomography study. Clin Experi-ment Ophthalmol. 2008;36:812-816.

18. Schumann RG, Schaumberger MM, Rohleder M, et al. Ultra-structure of the vitreomacular interface in full-thickness idiopathic macular holes: a consecutive analysis of 100 cases. Am J Ophthalmol. 2006;141:1112-1119.

19. Ito Y, Terasaki H, Takahashi A, Yamakoshi T, Kondo M, Nakamura M. Dissociated optic nerve fiber layer appearance after internal limit-ing membrane peeling for idiopathic macular holes. Ophthalmology. 2005;112:1415-1420.

20. Alkabes M, Salinas C, Vitale L, Burés-Jelstrup A, Nucci P, Mateo C. En face optical coherence tomography of inner retinal defects after in-ternal limiting membrane peeling for idiopathic macular hole. Invest Ophthalmol Vis Sci. 2011;52:8349-8355.

21. Clark A, Balducci N, Pichi F, et al. Swelling of the arcuate nerve fiber layer after internal limiting membrane peeling. Retina. 2012;32:1608-1613.

22. Haritoglou C, Ehrt O, Gass CA, et al. Paracentral scotomata: a new finding after vitrectomy for idiopathic macular hole. Br J Ophthalmol. 2001;85:231-233.

23. Ehlers JP, Gupta PK, Farsiu S, et al. Evaluation of contrast agents for enhanced visualization in optical coherence tomography. Invest Oph-thalmol Vis Sci. 2010;51:6614-6619.

Intraoperative SD-OCT in Macular Surgery

Documents

Transcript of Intraoperative SD-OCT in Macular Surgery