Assessment of Reading Behavior with an Infrared Eye...

Assessment of Reading Behavior with an Infrared EyeTracker after 360° Macular Translocation forAge-Related Macular Degeneration

Gurmit Uppal,1,2 Mary P. Feely,1,2 Michael D. Crossland,1,2 Luke Membrey,1 John Lee,1

Lyndon da Cruz,1,2 and Gary S. Rubin2,3

PURPOSE. Macular translocation (MT360) is complex surgeryused to restore reading in exudative age-related macular degen-eration (AMD). MT360 involves retinal rotation and subsequentoculomotor globe counterrotation and is not without signifi-cant surgical risk. This study attempts to gauge the optimalpotential of MT360 in restoring reading ability and describe thequality and extent of recovery.

METHODS. The six best outcomes were examined from a con-secutive series of 23 MT360 cases. Reading behavior and fixa-tion characteristics were examined with an infrared eyetracker. Results were compared to age-matched normal sub-jects and patients with untreated exudative and nonexudativeAMD. Retinal sensitivity was examined with microperimetry toestablish threshold visual function.

RESULTS. MT360 produced significant improvements in visualfunction over untreated disease and approximated normal func-tion for reading speed and fixation quality. Relative to the com-parative groups, eye tracking revealed the MT360 cohort gener-ated a greater number of horizontal and vertical saccades, oflonger latency and reduced velocity. In contrast, saccadic behav-ior when reading (forward and regressive saccades) closelymatched normal function. Microperimetry revealed a reduction inthe central scotoma with three patients recovering normal fovealsensitivity.

CONCLUSIONS. Near normal reading function is recovered de-spite profound surgical disruption to the anatomy (retinal/oculomotor). MT360 restores foveal function sufficient to pro-duce a single stable locus of fixation, with marked reduction ofthe central scotoma. Despite the limitations on saccadic func-tion, the quality of reading saccadic behavior is maintainedwith good reading ability. Oculomotor surgery appears not tolimit reading ability, and the results of retinal surgery approx-imate normal macular function. (Invest Ophthalmol Vis Sci.2011;52:6486–6496) DOI:10.1167/iovs.10-5879

Difficulty in reading is the commonest disability reportedsecondary to central visual loss from macular disease. The

ability to read is a highly valued task, and its loss is linked to

considerable psychological and social distress and a markedreduction in quality of life.1–6

Exudative age-related macular degeneration (wet AMD) is acommon, rapid cause of central vision loss. Recent advances inantivascular endothelial growth factor (VEGF) treatments haveoffered the possibility of reversal of vision loss. In severe lesions,notably where there is significant disruption of the retinal anat-omy (e.g., large subretinal hemorrhages, a large pigment epithelialdetachment, or retinal pigment epithelial tears with “scrolling”of the epithelium), anti-VEGFs are ineffective, and treatmentsoptions are limited to surgical methods designed to restorenormal anatomy (macular translocation or retinal pigment ep-ithelial transplantation) or visual rehabilitation. In terms ofvisual recovery, a primary goal of such treatments is the resto-ration of reading capability.

Conventional rehabilitation with low visual aids tries torestore reading capability by use of magnification. Despitemagnification, reading speeds are often limited to �50 wordsper minute, well below the level required for fluent reading(�80 words per minute).7,8 Macular translocation surgery(MT360) has been used to restore reading vision in severe wetAMD. MT360 attempts to rescue foveal photoreceptors beforeirreversible retinal atrophy/damage has occurred, re-establishnormal subfoveal anatomy, and provide stable, improved cen-tral vision.

Good visual outcomes have been reported when MT360 isperformed during the window of opportunity for treatmentthat corresponds to the period of viability of neurosensorycells.9–13 In most studies, outcome measures have concen-trated on distance acuity rather than near visual function orreading speed. Of note, Eckardt et al.9 and Lai et al.10 reportedimprovements in near acuity after translocation; Fujikado etal.14 specifically examined reading ability after MT360 andreported an improvement in critical print size (CPS), deter-mined with a Japanese version of the Minnesota Acuity Chart(MN Read—J Chart); and Toth et al.15 investigated variousparameters of near visual function after translocation and re-ported significant improvements in near acuity, contrast sensi-tivity, and reading speed.

This study was conducted to demonstrate the optimalpotential of MT360 in the restoration of normal visual func-tion by describing the quality and extent of this recovery.We observed the best-outcome cases from a series of 23consecutive patients with subfoveal choroidal neovascularmembrane (CNV) treated with MT360. MT360 is an invasiveand involved procedure (new foveal location, extraocularmuscle surgery, and residual torsion), and documenting thepotential for restoration of close to normal function is valu-able. We documented not only the well-recognized compo-nents of near visual function (reading acuity, contrast sen-sitivity reading speeds, and CPS) but with the use of a aninfrared eye tracker and microperimetry, we examined sac-

From the 1Moorfields Eye Hospital, London, United Kingdom; the2Institute of Ophthalmology, London, United Kingdom; and the 3Biomed-ical Research Centre for Ophthalmology, London, United Kingdom.

Supported by the Special Trustees of Moorfields Eye Hospital.Submitted for publication May 13, 2010; revised November 2, 2010,

and January 16 and February 20, 2011; accepted February 26, 2011.Disclosure: G. Uppal, None; M. Feely, None; M. Crossland,

None; L. Membrey, None; J. Lee, None; L. da Cruz, None; G.S.Rubin, None

Corresponding author: Gurmit Uppal, Moorfields Eye Hospital,162 City Road, London EC1V UK; [email protected].

Retina

Investigative Ophthalmology & Visual Science, August 2011, Vol. 52, No. 96486 Copyright 2011 The Association for Research in Vision and Ophthalmology, Inc.

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cadic behavior when reading (number, duration, velocity,and direction of saccades), fixation characteristics (pre-ferred retinal loci and stability of fixation), and retinal sen-sitivity (size, location, and density of any postoperativescotoma), and compared these parameters to both untreateddisease and normal function.

METHODS

Patients and Ethical Approval

Six patients (3 women, 3 men; age range, 61–74) recruited from aseries of 23 consecutive patients (15 women, 8 men; age range,61–94 years), with second-eye subfoveal CNV secondary to severeAMD, underwent uncomplicated MT360 with silicone oil tampon-ade (surgeon LDC). Six weeks later, the procedure was completedwith combined counterrotation surgery (surgeon, JL) and removalof the oil (surgeon, LDC). All surgeries were performed at Moor-fields Eye Hospital, London between May 2003 and January 2006.

Central to this study was the assessment of reading behavior andfixation with an infrared eye tracker (see below). The eye trackerassessment involved performing tasks that requiring good readingability. Recruitment from the main surgical series was based onpatients who achieved improved or stable distance and readingvision, and a distance and reading acuity of logarithm of minimalangle of resolution (logMAR) of 0.70 or better. Ten patients metboth these criteria; however, four were excluded because theywere not able to cooperate with the testing requirements of thestudy because of the onset of multi-infarct dementia,1 disablingpersistent postoperative torsion,1 CNV recurrence,1 or difficultiesrelated to transport to the testing center.1 The six remaining rep-resented the best outcomes from the surgical series, and all patientswere able to perform the reading and fixation tasks described later.

No patient had diagnosed neurologic or psychiatric disease or otherocular comorbidity. All patients spoke English as a first language andwere able to give informed consent. The study conformed to theDeclaration of Helsinki, and the ethics committee of Moorfields EyeHospital gave their approval for the study to take place.

Preoperative Assessment and Follow-up

Patients underwent a complete ophthalmic assessment before sur-gery at day 1 and after surgery at 12 months. The assessmentconsisted of best corrected visual acuity (BCVA), reading acuity andspeed, contrast sensitivity, slit lamp biomicroscopy, Goldmann ap-planation tonometry, ophthalmoscopy, slit lamp assessment of fo-veal fixation, color fundus photography, scanning laser ophthalmo-scope (SLO) autofluorescence, indocyanine green and fluoresceinangiography, and optical coherence tomography (Table 1).

Distance Acuity. The BCVA was measured with a back-illumi-nated standard Early Treatment of Diabetic Retinopathy Study (ETDRS)chart (Lighthouse Low Vision Products, Long Island City, NY) at 4 mand recorded as a logMAR score.

Reading Acuity. The Minnesota Reading Acuity Chart (MNRead; Precision Vision, La Salle, IL) was used to assess readingperformance: reading acuity (smallest print that can be read withoutsignificant errors), CPS (smallest print that can be read with maxi-mum speed), and reading speed (maximum reading speed when notlimited by print size). Reading acuity and CPS were recorded aslogMAR scores and reading speed as words per minute (wpm).

Contrast Sensitivity. Contrast sensitivity was measured usingthe Pelli-Robson Contrast Sensitivity Chart (Clement Clarke Inc.,Columbus, OH) to assess contrast sensitivity at different spatialfrequencies.

Color Fundus Photography and Angiography. Allcolor fundus photographic and angiographic images were taken andprocessed with a retinal camera (TRC-50IX; Topcon Medical Sys-tems, Inc., Paramus, NJ). T

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IOVS, August 2011, Vol. 52, No. 9 Eye Tracker Analysis of Reading after Retinal Rotation 6487


SLO Autofluorescence. An autofluorescence scan of the pos-terior pole was performed on all patients with a confocal scanninglaser ophthalmoscope (Retina Angiograph 2 HRA2; Heidelberg Engi-neering, Dossenheim, Germany).

Slit-Lamp Assessment of Fixation. A simple, five-step, slitlamp–based system was used to assess the quality of foveal fixation(Appendix).16 Fixation was classified on the basis of the results asfoveal, unstable, or no foveal fixation.

Infrared Eye Tracker Assessment of Readingand Fixation

Eye Movement Recording. Eye movements were measuredwith a commercial system (Eyelink Gazetracker; SensoMotoric Instru-ments, Teltow, Germany, running EyeLink Software, ver. 2.04). Thesystem is a headband-mounted apparatus equipped with two adjust-able infrared cameras that record eye position by using the “brightpupil” technique. A third camera on the headband tracks head motionby monitoring infrared emitters positioned at the corners of a high-resolution display monitor (21-in. Trinton GDM-F500R; Sony Corp.,Tokyo, Japan), with a resolution of 800 � 600 pixels and a refreshfrequency of 85 Hz. The luminance of the white background of thescreen was 125 cd/m2. The patients were seated 50 cm from themonitor and wore suitable refractive correction for the screen dis-tance. With this arrangement, compensation for head motion wasmade so that a real position of gaze could be calculated. Eye positionwas measured at a temporal resolution of 250 Hz, with a gaze positionaccuracy of �0.5°, according to the manufacturer.

Before each assessment, eye tracker calibration, validation, anddrift correction were performed using the algorithms provided for thispurpose. Only trials where calibration was categorized as good by thesoftware were included. Saccades were defined as being eye velocitymovements with velocity �30 deg/s�1 or acceleration �8000 deg/s�2

and described in terms of their number, average latency, averagevelocity, and direction (horizontal, vertical, forward, and regressive).

Reading Assessment. A full description of the eye trackerassessment of reading is given in the literature.17,18 Briefly, a readingtask was performed by using 10 randomly selected sentences consist-ing of 10 words and a 150-word paragraph displayed on the computermonitor. The sentences were displayed in Times New Roman font, ata Flesch-Kincaid reading grade of 8.0, presented at the optimal text sizefor the patient according to their CPS, as determined by their perfor-mance on the MN Read Chart.

Assessment of Preferred Retinal Locus/Loci and Fixa-tion Stability. A full description of the eye tracker assessment offixation stability is given in the literature.17–20 Briefly, fixation stabilitywas recorded while patients fixated a target presented for 10 secondsin each of five locations, in a randomized order. The target was a roundblack disc of 3° diameter with an 18-minute white central detaildisplayed against a white background.

The data collected were used to describe fixation by calculating abivariate contour ellipse, as described in the literature.17–21 A bivariatecontour ellipse describes the locus of fixation in normal observers. Thearea of this ellipse—the bivariate contour ellipse area (BCEA)—indi-cates fixation stability. The BCEA of normal individuals is approxi-mately 80 to 1200 min arc2 and, with macular disease, it ranges fromnear normal to over 13,000 min arc2.22 A nonparametric modelingtechnique (the kernel density estimator) was used to assess whetherindividual BCEAs provided a better fit to the data than a global BCEA.This analysis was used to determine the number of preferred retinalloci (PRL).

Assessment of Horizontal and Vertical Saccades. A fulldescription of the eye tracker assessment of horizontal and verticalsaccades is given in the literature.17,18 Briefly, horizontal and verticalsaccades were assessed while patients followed a simple fixation target(a round black disc of 3° diameter with an 18-minute white centraldetail displayed against a white background), from left to right forhorizontal saccades and from top to bottom for vertical saccades.

Eye Tracker Control/Comparative Data Groups. Datacollected from eye tracker assessment after MT360 were comparedwith similar data collected from normal controls (normal), patientswith dry AMD, and patients with wet AMD. Each group contained 10age-matched patients who underwent the aforementioned eye trackerassessment of reading and fixation (Table 2).

Microperimetry Assessment of Retinal Sensitivityand Fixation

The size of any postoperative scotoma was measured with a micrope-rimeter (MP-1 Microperimeter; Nidek Co., Ltd., Gamagori, Japan), a fulldescription of which is given in the literature.23 Briefly, the patientswere asked to fixate a central cross while responding, by means of abutton press, when they saw a point target presented at a retinallocation. The stimuli used were Goldmann III size targets of 200-cd/mintensity 2 and were presented for 200 ms. Identification of a retinallandmark enabled a scotoma map to be superimposed onto a retinalimage.

Before each assessment, patients also underwent an objective fix-ation analysis with the microperimeter. Using a 1° single white crosstarget of 200-cd/m2 intensity patients were asked to fixate the targetfor 30 seconds. Identification of a retinal landmark enabled the fixationanalysis to be superimposed onto a retinal image.

Surgical Technique

All surgeries were performed in patients under general anesthesia by asingle surgeon: macular translocation and removal of silicone oil (LDC)and counterrotation surgery (JL).

Macular Translocation. Macular translocation (MT360) wasperformed as described by Eckardt et al.9

Globe Counterrotation. Counterrotation of the translocatedeye was performed with removal of silicone oil approximately 6 to 8weeks after retinal rotation surgery. In all patients, the retina wasrotated superiorly, requiring excyclotorsion of the globe. This wasachieved with surgery on the oblique muscles combined with trans-position of the medial and lateral recti. Counterrotation surgery pro-duced a postoperative median incyclotorsion of 5° (0°–10°), with nopatients reporting symptoms of diplopia or tilt (Table 1).

Statistical Methods

Descriptive statistics (n, median, range, minimum, maximum, andinterquartile range) were obtained for each data set (MT360 cohort andthe control/comparative groups). The data sets were examined forsignificant differences in ETDRS acuity, MN Read reading acuity, MNRead CPS, MN Read critical print reading speed, Pelli-Robson contrastsensitivity, eye tracker reading speed, horizontal and vertical saccades,saccadic speed and latency, global fixation, and number of preferredPRLs. Statistical analysis was performed with the Mann-Whitney test(SPSS statistical software; SPSS, Inc., Chicago, IL). All outcome mea-sures quoted herein represent median values, unless otherwise stated.

TABLE 2. Control/Comparative Group Demographics

Group nMean Age,y (range) Diagnosis n

Normal 10 71.0 (62–79) No pathologyDry AMD 10 76.2 (62–84) Geographic atrophy 9

Macular drusen 1Wet AMD 10 79.2 (74–85) CNV 7

PED 3MT360 6 68.7 (61–74) CNV 6

PED, pigment epithelial detachment.

6488 Uppal et al. IOVS, August 2011, Vol. 52, No. 9


RESULTS

MT360 Acuity Outcomes

Surgical Series. The ETDRS distance and MNRead acuityoutcomes for the surgical series of 23 patients (15 women, 8men; age range, 61–94 years) treated with MT360 are illus-trated in Figure 1.

Distance Acuity. At 12 (04–36) months’ follow-up, themean postoperative distance acuity (range) improved fromlogMAR 0.90 (0.18–2.1) to 0.67 (0.10–1.80; P � 0.05). Aftersurgery, the distance vision improved in 14 (60.9%) patients bygreater than 0.1 logMAR, remained unchanged within 0.05logMAR of the preoperative acuity in 5 (21.7%) patients, anddeteriorated by greater than logMAR 0.1 in 4 (17.4%) patients.Before surgery, 48% of patients had a distance acuity of logMAR�0.7 (20/100 or better), and 4% a distance acuity of logMAR�0.3 (20/40 or better). After surgery this improved to 69%with a distance acuity of logMAR �0.7 (20/100 or better), 26%with a distance acuity of logMAR �0.3 (20/40 or better), and39% with a 3-line gain in visual acuity.

Reading Acuity. For the same period, the mean postoper-ative reading acuity (range) improved from logMAR 1.21(0.60–2.00) to 0.91 (0.22–2.00; P � 0.05). After surgery, thereading acuity improved in 15 (65.2%) patients by greater than0.1 logMAR, remained within 0.05 logMAR of the preoperativeacuity in 4 (17.4%) patients, and deteriorated by greater than0.1 logMAR in 4 (17.4%) patients. Before surgery, 13% ofpatients had a reading acuity of logMAR �0.7 (N10 or better),no patients had an acuity of logMAR �0.3 (N5), with the bestpreoperative reading acuity recorded at logMAR 0.6 (N8) in asingle patient. Before surgery, 52% of patients had a readingacuity of logMAR �0.7 (N10), 17% a near acuity of logMAR�0.3 (N5), and 61% a gain of 0.3 logMAR.

Eye Tracker MT360 Cohort

The six best available outcomes (three women, three men; agerange, 61–74) from the aforementioned series were recruitedto investigate post-MT360 reading behavior (Table 1). At 14(5–29) months of follow-up, in this cohort (MT360 cohort),surgery improved the postoperative distance acuity from log-MAR 0.70 (0.44–1.80) to 0.25 (0.10–0.65; P � 0.05), and thecontrast sensitivity (range) from logMAR 0.75 (0–1.05) to 1.43(1.20–1.65; P � 0.02). In terms of reading function, the post-operative reading acuity improved from logMAR 1.02 (0.60–1.43) to 0.52 (0.22–0.66; P � 0.01), the reading speed from

107 (52–150) to 158 (55–231) wpm (P � 0.05), and the CPSfrom logMAR 1.10 (1.10–1.20) to 0.80 (0.50–1.10; P � 0.05).

The relationship between distance and reading acuity, be-fore and after MT360, is summarized in Figure 2. Preoperativedistance acuity correlated well with reading acuity (r ��0.71); however, no such correlation was found with CPS (r ��0.04). After surgery both the reading acuity and CPS signifi-cantly improved, and both parameters correlated well with thepostoperative distance acuity (Fig. 2).

Comparison of Visual Function: MT360 versusNormal versus AMD

Distance Acuity, Reading Function, and Contrast Sen-sitivity. Outcome measures (distance and reading acuity andreading speed) for the MT360 cohort and the comparativegroups are summarized in Figure 3. The trend for each measurewas for postoperative function for the MT360 cohort to begreater than that of both untreated AMD groups and less thanthe age-matched normal group. This difference in functionbetween the MT360 cohort and the AMD groups reachedsignificance (P � 0.05) for all parameters except CPS andcontrast sensitivity. Similarly, the difference in function be-tween MT360 cohort and age-matched normal subjectsreached significance (P � 0.05) for all parameters exceptreading speed (Fig. 3).

Eye Tracker Assessment of Reading Function. Horizon-tal Saccade Task. Assessment of horizontal saccades in responseto a fixation target demonstrated that the MT360 cohort per-formed a greater number of saccades (MT360 2.44) than thecomparative groups (normal 2.00, P � 0.05; dry AMD 1.84, P �0.05; and wet AMD 2.35, P � 0.05). Examining saccade duration,the latency was longer for the MT360 cohort (269 ms) than thecomparative groups (normal 225 ms, P � 0.05; dry AMD 238 ms,

FIGURE 2. Relationship between distance acuity and reading function.The charts illustrate the relationship between distance acuity andreading function (acuity and CPS). A comparison of the preoperative(A) and postoperative (B) data reveals the restoration of reading func-tion after MT360 and the reestablishment of the association betweendistance and near function.

FIGURE 1. Surgical group: acuity outcomes. ETDRS distance and MN-Read reading acuity outcomes after MT360 in a series of 23 consecutivepatients. The patients selected for assessment with the eye tracker arenumbered and highlighted with solid data points (Table 1).



P � 0.05; and wet AMD 209 ms, P � 0.05). Finally, saccadevelocity was slower for the MT360 cohort (364 ms�1) comparedwith the other groups (normal 479 ms�1, P � 0.05; dry AMD 459ms�1, P � 0.05; and wet AMD 470 ms�1, P � 0.05; Table 3).

Vertical Saccade Task. A similar pattern of results wasobserved for vertical saccades, with the MT360 cohort per-forming a greater number of saccades of increased latency andslower velocity (Table 3).

Reading Task. Saccadic assessment when reading revealedthat the MT360 cohort displayed a greater number of forward

saccades (13.5) than the age-matched normal group (8.7, P �0.05) but less than the dry (17.3, P � 0.05) and wet (29.1, P �0.05) AMD groups. There was no significant difference be-tween the groups for the number of regressive saccades per-formed (MT360 29.4; normal 31.5, P � 0.05; dry AMD 12.0,P � 0.05; and wet AMD 33.0, P � 0.05; Table 3).

Reading Speeds. Assessment of reading speeds revealed thatthe MT360 cohort read at a speed (101 wpm) that approxi-mated that of the normal group (139 wpm, P � 0.05) and at agreater speed than that of the AMD groups (dry 79 wpm, P �0.05; wet 39 wpm P � 0.05). Reading speeds, as calculatedfrom MN Read Reading Acuity Charts revealed a similar pattern(MT360 158 wpm; normal 151 wpm, P � 0.05; dry AMD 94wpm, P � 0.05; and wet AMD 51 wpm, P � 0.05).

Eye Tracker Assessment of Fixation. The global BCEAvalues for the MT360 cohort (310 min arc2) were closer to thenormal group (116 min arc2; P � 0.05) than the AMD groups(dry AMD 1426 min arc2; P � 0.05; wet AMD 651 min arc2; P �0.05), no statistically significant difference was found betweenthe MT360 cohort and any comparative group. Analysis offixation stability revealed a single preferred retinal loci for theMT360 cohort and the age-matched normal subjects (P � 0.05)with multiple loci for both AMD groups (P � 0.05).

The aforementioned eye tracker data revealed several sig-nificant results and patterns; however, it must be emphasizedthat nonsignificant results suggest only a trend. Furthermore,the sample sizes limit the ability to regard one test or group asconsiderably different from another.

Microperimetry Assessment of Retinal Sensitivity andFixation. Retinal Sensitivity. Microperimetry assessment(MP-1; Nidek) of macular sensitivity demonstrated that in three(patients 1, 3, and 4) of the six patients in the MT360 cohort,surgery restored near normal levels of foveal and parafovealretinal sensitivity (Fig. 4). Only patient 6 demonstrated a sig-nificant residual absolute central scotoma.

Fixation. Microperimetry fixation analysis demonstratedhigh-quality, stable fixation for all patients in the MT360 co-hort. The mean percentage of time that the target was placedwithin 2° of the fovea over the 30 seconds of the test periodranged from 78% to 100% (Fig. 4). Pre- and post-MT360 BCEAvalues from the perimeter are also shown for comparison.

TABLE 3. Saccadic Function: MT360 versus Comparative Groups

Groups MT360 Normal Dry AMD Wet AMD

Horizontal Saccades

Number of saccades 2.44 2.00 1.84 2.35P � 0.009 P � 0.008

Latency/ms 269 225 238 209Velocity/ms�1 364 479 459 470

P � 0.050 P � 0.013 P � 0.023

Vertical Saccades

Number of saccades 2.32 1.76 2.20 2.09P � 0.044

Latency/ms 249 197 217 234P � 0.039

Velocity/ms�1 378 446 404 378

Reading Saccades

Forward saccades 13.5 8.7 17.3 29.1P � 0.002 P � 0.002

Regressive saccades 29.4 31.5 12.0 33.0

Data are a comparison of parameters of saccadic function betweenthe MT360 cohort and each of the control/comparative groups. Thevalues represent the median result.

FIGURE 3. Distance acuity and reading MT360 cohort versus compar-ative groups. The charts compare the visual parameters of distanceacuity (A), reading acuity (B), and reading speed (C) between theMT360 cohort and each of the control/comparative groups. The boxplots display the median value, the range, and the SD for each group.P values are highlighted to show results reaching a statistical difference(P � 0.05).



FIGURE 4. Microperimeter (MP-1;Nidek, Gamagori, Japan) assessmentof post-MT360 retinal sensitivity andfixation analysis. Shown for each pa-tient, the recovery of retinal sensitiv-ity and fixation after MT360. For themacular sensitivity images, the areasof peripheral scotoma in red repre-sent nonfunctional retinal areas over-lying the original site of subfovealpathology. Foveal sensitivity mapsshow the extent of recovery of cen-tral function and both sets of sensi-tivity maps are overlaid with the fix-ation analysis taken at the time. Aseparate fixation analysis is also illus-trated and the percentage of time thetarget is placed within 2° and 4° ofthe fovea during the 30 seconds ofthe test is illustrated along with theperimetric classification of fixation.All patients demonstrated high qual-ity fixation, classified as greater than50% of the preferred fixation pointslocated within a 2° diameter circlecentered on the fovea. Finally, foreach patient the pre- and postopera-tive BCEA values generated from theperimeter are also illustrated demon-strating either significant improve-ment in fixation or maintenance ofgood preoperative fixation.



DISCUSSION

MT360 differs from current treatments for severe AMD that areintended to modify the disease process. Instead, translocationoffers a unique rescue procedure for foveal photoreceptors inpatients whose fellow eye has already lost central vision. Pre-vious reports of translocation have reported this rescue interms of acuity alone.9,12,24 More recently, several groups haveexamined the impact of MT360 on near visual function andreading ability.10,13–15,25 Although these studies provide goodevidence for the recovery of foveal photoreceptor function bymidperipheral retinal pigment epithelium (RPE), none has de-scribed the quality and extent of this recovery compared withnormal visual function.

MT360 is a complex procedure encompassing both retinaland strabismus surgery. It is not without significant surgicalrisk, including endophthalmitis, proliferative vitreoretinopathy(PVR) and associated retinal detachment, choroidal hemor-rhage, and anterior segment ischemia. Although improvementsin the surgical technique and vitreoretinal instrumentationhave considerably reduced some of these risks, particularlyPVR detachment, total loss of sight remains a possibility sec-ondary to these complications. Nevertheless, MT360 remainsthe only treatment modality to offer retinal reconstruction forsevere neovascular AMD, in which there is gross mechanicaldisruption of retinal architecture not amenable to the currentgeneration of medical AMD therapies.

The results of the first 23 consecutive patients treated withMT360, a series that includes the surgical learning curve, illus-trated a significant restoration of both distance and readingacuity (Fig. 1). MT360 led to 39% of patients gaining three linesof distance acuity and 61% gaining 0.3 logMAR of readingacuity, with 17% achieving a near acuity of logMAR �0.3 (N5)compared with no patients reading at this level before surgery.These results compare favorably with those in previous inves-tigations into MT360.9,10,12–15 From this series, we examinedthe best-outcome cases, to gauge the optimal potential of thiscomplex surgery to restore normal function. Best-outcomecases represented patients who achieved improved or stabledistance and reading vision and a distance and reading acuity oflogMAR 0.7 or better. These criteria were set to recruit onlythose patients capable of meeting the demands of the eyetracker and microperimetry assessments. Ten (43.5%) patientsmet both these criteria from the surgical series in which 69%achieved a distance and 52% a reading acuity of logMAR 0.7 orbetter, with four patients excluded for reasons outlined in theMethods section.

At the 14-month follow-up, the measured parameters ofvisual function all improved or remained relatively stable in thiscohort (Table 1). As with the main surgical series, the observedtrend was for a greater improvement in near than in distancefunction. Several studies of MT360 have reported similar find-ings.9,10,13,14 Other than sample size, the discrepancy in nearcompared with distance vision is difficult to explain and mayreflect the complex interplay of location, density, and size of aresidual scotoma on reading function. A possible explanation isthat MT360 results in a reduction in the foveal scotomatousarea, without an improvement in overall retinal sensitivity, thusresulting in a greater improvement in near function. In addi-tion, alterations in microsaccadic behavior after counterrota-tion surgery (discussed below) may have more of a deleteriouseffect on distance acuity than near reading ability.

The failure of reading speed (which is not limited by printsize) to improve significantly reflects the fact that a reasonablespeed may be attained before surgery (at a larger print size) andonly marked improvements in this parameter will reach signif-icance. In this respect, the CPS (smallest print read with max-

imum speed), which significantly improved after MT360, bet-ter reflects improvements in reading ability (Table 1).

Before surgery distance acuity correlated well (r � �0.71)with reading acuity as expected; however, there was no suchcorrelation (r � �0.04) with CPS (Fig. 2). Patients have aprofound central scotoma in their previously better secondeye, and it is predominately the loss of reading ability and notdistance acuity that commonly instigates presentation. Thepoor reading capability stems from the scotoma forcing eccen-tric viewing,25 an unstable locus for fixation,17,21,26,27 andcompromised eye movement control.28–30 In the long term,patients may develop adaptive mechanisms to partially over-come these problems; however, a requirement of successfulMT360 is a short duration between acute visual loss and sur-gery.16 Thus, before surgery, although patients may still resolvesmaller print sizes, the CPS remains relatively poor and inde-pendent of distance and reading acuity. This result again dem-onstrates that both distance and reading acuity are inadequatemeasures of reading capability.

After surgery, distance acuity was well correlated with boththe reading acuity (r � �0.79) and CPS (r � �0.91; P � 0.001;Fig. 2). Surgery dramatically reduced or reversed the absolutecentral scotoma, recovering levels of macular sensitivity ap-proaching normal with stable central fixation (Fig. 4). MT360resulted in foveal anatomy that closely approximates a normalphysiological state, and this is reflected in significant improve-ments in function (reading acuity, CPS, and contrast sensitivity)and hence reading ability. These results support the premisethat restoration of the choriocapillaris–Bruch’s–RPE–photore-ceptor axis rescues foveal function, and this can be achievedwith the midperipheral RPE substituting for the diseased sub-foveal RPE.

To gauge the extent of the recovery detailed above, out-come measures (distance acuity, reading acuity, reading speed,CPS, and contrast sensitivity), eye tracker assessment of read-ing behavior, and microperimetry were examined, comparing,where possible, the MT360 cohort with age-matched normalsubjects and patients with untreated wet and dry AMD. Thecomparison revealed a pattern indicating that the recovery offunction after MT360 was greater than either of the untreatedAMD groups and less than the age-matched normal group (Fig.3, Table 3). The results were consistent with an improvementin the absolute central scotoma with restoration of the macularthreshold function and resolution of the size and/or density ofthe preoperative scotoma. As microperimetry was not availablebefore surgery, changes in retinal threshold function could notbe quantified directly; however, all patients in the surgicalcohort presented with large a subfoveal hemorrhage and arecent loss of reading capability. Although microperimetryrevealed that surgery returns macular sensitivity toward normallevels, a relative scotoma persists (Fig. 4). This residual sco-toma is likely to account for reduced reading ability and wouldalso explain the failure of the surgical cohort to match out-comes comparable to normal, except for reading speed. Asdiscussed earlier, although CPS better reflects reading ability, itis of interest to note that, after translocation and counterrota-tion, patients were able to recover sufficient function toachieve a normal level of maximum reading speed (Fig. 3).

In addition to near normal levels of macular sensitivity,patients 1, 3, and 4 also displayed the best three postoperativeoutcomes (Table 1). Of note, patient 1 had the best preoper-ative vision, whereas patients 3 and 4 had the worst. This resultsuggests that although good preoperative vision will, as ex-pected, result in good postoperative outcomes, the major de-terminant for any rescue procedure is likely to be the numberand quality of the foveal photoreceptor pool before surgery.Thus, in the present surgical series, case selection was based



primarily on the degree of residual foveal function and not onacuity.16

MT360 is intended to restore function by reestablishingretinal anatomy, and so the health of the underlying chorio-capillaris–Bruch’s–RPE bed that receives the fovea is equallycritical to the success of the procedure. In MT360, the fovea iscustomarily superiorly rotated 20° to 30° and after surgery liesat the margins of the original macular RPE bed. It is known thatloss of function is matched by changes in the underlyingchoriocapillaris–Bruch’s–RPE complex.31–33 As such, a de-tailed assessment of foveal, parafoveal, and paramacular RPEfunction may further improve case selection and surgical out-comes. In the present surgical series autofluorescence wasperformed to give a measure of macular and paramacular RPEfunction; however, multifocal ERG or microperimetry may beadditional investigations that assist in determining the degreeof subfoveal support likely to be available at the recipientsite.34–37 Furthermore, the macula consists of a cone-domi-nated fovea surrounded by a rod-dominated parafovea andmeasures of scotopic, photopic, and chromatic sensitivitiesmay further determine the degree of residual function andsupport before surgery. To date, a wealth of studies havedescribed the loss of central macular structure and function,particularly early cone damage, as well as the involvement ofwider retinal areas in AMD than are evident from funduscopy(Hageman GS, et al. IOVS 2002;43:ARVO E-Abstract1988.31,34–49 Ideally, these factors need to be considered todetermine the degree and extent of preexisting disease andestablish the baseline retinal health from which recovery isattempted.

Practically, when patients presented with disease secondeyes, case selection for the MT360 surgical series was based ona rapid clinical assessment of residual foveal function. This wasdetermined from the duration of symptoms and performanceon a foveal fixation task (Appendix) and not the presentingacuity.16 Patients with symptoms beyond 12 weeks were ex-cluded, as were those who did not demonstrate good fovealfixation. It could be argued that duration of visual loss could beused without assessing fixation behavior, as intuitively the twoparameters are related. However, simply using duration ofvisual loss to predict outcomes would not identify which pa-tients were still within the critical window of opportunity torecover residual photoreceptor function. Although this criticalwindow was estimated to be in the region of 12 weeks, theexact duration depended on the number of remaining viablephotoreceptors at presentation and the severity and course ofthe disease process. Thus, patients with a slow, insidious dis-ease course would be expected to have a smaller pool of viablefoveal photoreceptors at presentation than would patients pre-senting with a short overall disease onset. As such, fixationbehavior was an important determinant of the critical period ofphotoreceptor viability. When used together with time sinceacute visual loss, both parameters provided a powerful methodof assessing suitability for MT360 and good outcomes. Ideally,to indicate the contribution of the fixation task versus theduration of visual loss, an examination of cases where therewas a marked discordance between fixation behavior and du-ration of visual loss was required. As expected by the naturalhistory of the disease, no cases of good fixation and a markedlyextended period of visual loss were encountered, nor werethere any cases of poor fixation and immediate presentation.

With regard to the procedure itself, ultrastructural and elec-trophysiological studies have found a partial loss of photore-ceptor outer segments after translocation, thought to be tornaway during separation of the retina from the RPE.50–52 There-fore considering that surgical recovery is undertaken on thebackground of an ageing and diseased retina and that thephysical processes involved in MT360 will result in a further

loss of photoreceptors, recovery of truly normal function is lesslikely.

Eye tracker assessment of saccadic behavior revealed thattranslocation resulted in a greater number of horizontal sac-cades of reduced velocity and increased latency comparedwith that in with the other groups (Table 3). Examination ofvertical saccades, which are implicated in finding a new linewhen reading, revealed a similar pattern. A detailed examina-tion of horizontal saccades when reading revealed that theMT360 cohort displayed a greater number of forward saccadesthan the age-matched normal subjects but fewer than the AMDgroups, with no difference in the number of regressive sac-cades between groups (Table 3). Eye tracking and microperim-etry also established that MT360 restored a single stable centrallocus of fixation with BCEA values approaching normal sub-jects (Fig. 4). Thus, in the presence of high-quality stablefixation, these results reflect the direct effects of counterrota-tion surgery on gaze control during reading rather than deficitsin macular function. Counterrotation surgery (which involvestransposition of two to four recti muscles) is necessary tocorrect posttranslocation torsion to less than 10° (when it isconsidered that symptoms of diplopia and tilt are negligible).Despite the suboptimal oculomotor dynamics highlightedabove, the MT360 cohort still achieved near normal readingcapability.

The purpose of our study was to gauge the optimal poten-tial of MT360 in rescuing function and to describe the qualityand extent of the recovery. MT360 is a complex two-stageprocedure, after which patients have a reduced peripheral field(secondary to 360° retinectomy performed during retinal trans-location) and degree of residual torsion (secondary to counter-rotation surgery). Despite the profound anatomic (retinal andoculomotor) disruption that MT360 induces, the results indi-cate that the procedure’s results approximate normal macularthreshold levels with stable foveal fixation. Although eye track-ing identified that surgery quantitatively limited saccadic be-havior (number, velocity, and latency), these limitations onoculomotor control appear not to adversely affect qualitativesaccadic behavior (saccade direction) when reading, whichagain approximated that of normal subjects. It is acknowl-edged that the study findings are clearly limited by the smallsample size and the variability of the data set. Nevertheless, thepresent study demonstrates a clear rescue of photoreceptorsand identifies trends in saccadic activity when reading that arean improvement over untreated disease.

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APPENDIX

TABLE A1. Slit Lamp Assessment of Quality of Fixation

Instructions to Patient Target Task Slit Lamp View

Look at the spot of light 0.2-mm spot Fixes with Fovea�Maintains

fixation 1–3 s

Look at the top rightcorner of the square.

Repeat instruction for:bottom right corner,bottom left corner,top left corner

2 mm2 Projects to eachcorner ofsquare with asingle saccade

�Maintainsfixation 1–3 s

Look at the top of thebar.

Now look at the bottomof the bar.

Repeat once.

4 � 1-mm verticalslit

Fixes to top andbottom of slitwith a singlesaccade


Look to the left side ofthe bar.

Now look at the rightside of the bar.

Repeat once.

4 � 1-mmhorizontal slit

Fixes to left/right of slitwith a singlesaccade;


Look at the spot of light. 0.2-mm spot placedoutside lesion

Refixates tofovea with asingle saccade;


Failed task: defined as failure to follow instructions or maintain fixation for 1 to 3 seconds as outlined.



TABLE A2. Classification of Fixation Based on Slit Lamp Assessment

Slit Lamp Tasks Classification of Fixation

All tasks successfully completed Foveal (good) fixationTasks performed, but poorly Unstable (poor) fixationMore than a single saccade � fixates object for less than 1 secondUnable to complete any tasks No foveal fixation



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