ARTICLE

Dynamic imaging of accommodation by swept-source anterior segment optical coherence tomography Alberto Neri, MD, Marco Ruggeri, PhD, Alessandra Protti, MD, Rosachiara Leaci, MD, Stefano A. Gandolfi, MD, Claudio Macaluso, MD

PURPOSE: To study the accommodation process in normal eyes using a commercially available clinical system based on swept-source anterior segment optical coherence tomography (AS-OCT). SETTING: Ophthalmology Department, University of Parma, Italy. DESIGN: Evaluation of diagnostic technology. METHODS: Right eyes were analyzed using swept-source AS-OCT (Casia SS-1000). The optical vergence of the internal coaxial fixation target was adjusted during imaging to obtain monocular accommodation stimuli with different amplitudes (0, 3.0, 6.0, and 9.0 diopters [D]). Overlapping of real and conjugate OCT images enabled imaging of all the anterior segment optical surfaces in a single frame. Central corneal thickness (CCT), anterior chamber depth (ACD), and lens thickness were extracted from the OCT scans acquired at different static accommodation stimulus amplitudes. The crystalline lens was analyzed dynamically during accommodation and disaccommodation by acquiring sequential OCT images of the anterior segment at a rate of 8 frames per second. The lens thickness was extracted from the temporal sequence of OCT images and plotted as a function of time. RESULTS: The study analyzed 14 eyes of 14 subjects aged 18 to 46 years. During accommodation, the decrease in the ACD was statistically significant (P < .05), as were the increase in the lens thickness (P < .001) and the slight movement forward of the lens central point (P < .01). The CCT and anterior chamber width measurements did not change statistically significantly during accommodation. The lens thickness at 0 D was positively correlated with age (P < .01). CONCLUSION: High-resolution real-time imaging and biometry of the accommodating anterior segment can be effectively performed using a commercially available swept-source AS-OCT clinical device. Financial Disclosure: No author has a financial or proprietary interest in any material or method mentioned. J Cataract Refract Surg 2015; 41:501–510 Q 2015 ASCRS and ESCRS Online Video

Accommodation is the adjustment of the dioptric power of the eye to obtain clear retinal images while looking at objects at varying distances.1 A loss of near vision from age-related presbyopia or after cataract surgery is one of the most common ophthalmology patient complaints. Because of the considerable impact that a medical procedure for restoring accommodation could have on an aging population, there has been much interest in presbyopia research. Although the basic model of accommodation goes back to 1855,1 Q 2015 ASCRS and ESCRS Published by Elsevier Inc.

the accommodation and presbyopia mechanisms are not yet fully understood.2 Cross-sectional imaging technology for detailed evaluation of the eye in vivo and in real time is technically challenging but could help us to better understand the mechanisms of accommodation and presbyopia and thus lay the foundation for new procedures and implants for restoring dynamic accommodation. Magnetic resonance imaging,3–5 ultrasound biomicroscopy,6–8 and Scheimpflug camera–based http://dx.doi.org/10.1016/j.jcrs.2014.09.034 0886-3350

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optical systems5,9–11 have been used to study the anatomic changes in the eye during accommodation. In recent years, optical coherence tomography (OCT) has been used increasingly to study accommodation in vivo and in real time12–30 because it has several advantages over the other ophthalmic imaging technologies. Optical coherence tomography enables noncontact, high-speed, high-resolution imaging and biometry of ocular structures, is capable of 3-dimensional imaging, and can integrate coaxial accommodative targets to stimulate accommodation in physiologic conditions. Recently, a new implementation of OCT known as swept-source anterior segment OCT (AS-OCT) became available for clinical use.31–33 Swept-source AS-OCT is a time-encoded Fourier-domain OCT technology based on a wavelength-tunable laser source and has a very high imaging rate.34 Biometric measurements of the anterior segment structures performed by swept-source AS-OCT showed high reliability and repeatability.31–33 The present study showed that a commercially available swept-source AS-OCT (Casia SS-1000, Tomey Corp.) can be used for a high-resolution static and dynamic study of the anterior segment of the eye during accommodation. SUBJECTS AND METHODS The volunteer subjects provided written consent to enroll in the study, which was performed in accordance with the principles of the Declaration of Helsinki.35 Criteria for inclusion in the study were normal visual function and normal accommodation, emmetropic or slightly hyperopic refraction (spherical equivalent 0.5 diopter (D) to 1.0 D measured using the AR600 autorefractor, Nidek Co., Ltd.), and

Submitted: April 10, 2014. Final revision submitted: August 5, 2014. Accepted: September 8, 2014. Ophthalmology Department (Neri, Protti, Leaci, Gandolfi, Macaluso), Dipartimento di Scienze Biomediche, Biotecnologiche e Traslazionali, University of Parma, Parma, Italy; the Ophthalmic Biophysics Center (Ruggeri), Bascom Palmer Eye Institute, University of Miami Miller School of Medicine, Miami, Florida, USA. Supported by the Australian Government Vision Cooperative Research Centre, Sydney, Australia; the National Institutes of Health, Bethesda, Maryland (2R01EY14225, R01EY021834, P30EY14801), the Florida Lions Eye Bank, Miami, Florida, and Research to Prevent Blindness, New York, New York, USA (Dr. Ruggeri); and supported in part by funding from the University of Parma, Parma, Italy, and by grant “Programma di Ricerca Regione Universita” DGR22422007 (Drs. Neri, Protti, Leaci, Gandolfi, and Macaluso). Corresponding author: Alberto Neri, MD, Ophthalmology, University of Parma, Via Gramsci 14, 43126 Parma, PR, Italy. E-mail: [email protected].

uncorrected distance (Early Treatment of Diabetic Retinopathy Study tables, Precision Vision) and near (Runge Low Vision Near Card, Good-Lite Co.) visual acuities of better than 20/25 (!0.1 logMAR). The right eye of each subject was imaged using the Casia SS-1000 swept-source AS-OCT system. The OCT device has a swept-source laser that operates at a central wavelength of 1310 nm with an axial resolution of 10 mm (in tissue), a transverse resolution of 30 mm, and a scan rate of 30 000 A-scans per second. The transverse scanning pattern is customizable within a maximum area of 16.00 mm  16.00 mm, and the maximum imaging depth is 9.24 mm in air, which corresponds to approximately 6.0 mm in tissue. Simultaneous imaging of all the anterior segment structures, including the cornea, the aqueous humor, and the crystalline lens, is necessary to perform biometry of the accommodating eye.13,23,36 The imaging depth of the swept-source AS-OCT was not sufficient to image the anterior segment along its entire length, which would require an axial range of approximately 12.0 mm (in air). Figure 1 shows OCT vertical B-scans of the anterior segment of the eye representing the anterior (Figure 1, A) and posterior (Figure 1, B) portion of the anterior segment, respectively. To overcome this limitation, OCT scans of the anterior segment were acquired by overlapping the real and the complex conjugate (mirror) images produced by the system (Figure 1, C). The depth (z-axis) of the imaging axial range was adjusted to simultaneously include the anterior and posterior surfaces of the cornea and the lens, (Figure 1, C, points 1, 2, 3, and 4) in a single OCT frame. Because the image sensitivity is highest at the zero delay line, imaging was performed with the zero delay line near the posterior iris (the bottom of the OCT image at scan depth of 9.24 mm in air) to enhance the visualization of the lens. The OCT scans obtained using this technique showed a vertically inverted image of the posterior lens overlapping the direct image of the anterior structures (corneal, aqueous humor, and anterior portion of the lens). Although the internal structure of the lens was not clear, all the optical surfaces involved in the accommodation process were simultaneously displayed (Figure 1, C). For each subject, OCT scans were acquired using this image-overlapping technique at 4 static accommodation stimulus amplitudes (0 D, 3.0 D, 6.0 D, and 9.0 D). The scanning pattern consisted of 2 orthogonal transverse scans along the horizontal and the vertical meridians, each 16.0 mm long and consisting of 2048 A-scans. During image acquisition, subjects were asked to fixate on the coaxial accommodative target image in the OCT device. The amplitude was set using an automated system of swinging lenses inside the OCT device in front of the fixation target. The scans were excluded from further analysis if the subject indicated an inability to focus on the fixation target at a specific amplitude. The OCT system also has an integrated active eye tracker that automatically centers the axes of the horizontal (x) and vertical (y) transverse scans to the corneal reflex. The dynamic accommodative response to an accommodation stimulus stepped change from 0 D to 9.0 D was imaged in the same eye for each subject (Video 1, available at http:// jcrsjournal.org). An OCT video of dynamic accommodation for each subject also was recorded during a disaccommodation stimulus stepped change from 9.0 D to 0 D (Video 2, available at http://jcrsjournal.org). During the experiments, when image acquisition was starting, the participants were instructed to fixate on the coaxial target in the OCT

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Figure 1. Swept-source AS-OCT scans of an eye included into the study. A: Vertical B-scan showing the anterior part of the anterior segment. The posterior aspect of the crystalline lens is not part of the scan. B: Vertical B-scan showing the posterior part of the anterior segment. The entire crystalline lens is shown while the anterior part of the cornea is not included into the scan. C: Vertical B-scan showing the entire anterior segment by overlapping the real and conjugate images. The scan includes all the optical surfaces of the anterior segment, allowing the measurement of CCT (the distance in C from point 1 to point 2), ACD (the distance from point 2 to point 4), and lens thickness (the sum of the distances from point 4 to point 5 and point 3 to point 5).

device while the optical vergence of the accommodation target was changed. The eye was centered automatically by the active eye tracker of the OCT system. Each video involved 38 OCT horizontal and vertical scans acquired at an imaging rate of 8 frames per second for 4.625 seconds. For dynamic imaging, the scanning pattern was adjusted so that the transversal horizontal and the vertical scans were 12.0 mm long and consisted of 512 A-scans (Figure 2, A and B; Videos 1 and 2). From the images acquired along the vertical meridian, the linear measurements tool provided with the swept-source AS-OCT was used to determine the central corneal thickness (CCT), anterior chamber width (distance between the angular recesses), anterior chamber depth (ACD) (distance from the endothelium to the anterior surface of the crystalline lens along the fixation axis), and lens thickness (distance between the anterior and the posterior lens surfaces along the fixation axis). The lens central point (the sum of the CCT, the ACD, and one half of the lens thickness) and the anterior segment length (the sum of the CCT, the ACD, and the lens thickness) were calculated from the measurements. Lens thickness was measured and plotted as a function of time for the dynamic responses recorded during accommodation and disaccommodation. Geometric lengths were obtained by scaling the measured optical lengths using a group refractive index of 1.389 for the cornea and 1.343 for the aqueous humorA and an average refractive index of 1.421 for the crystalline lens.37 The anterior chamber width was measured on the same images after performing automated correction with the OCT software, which accounts for the difference between optical and geometric lengths and for the image warping at the different ocular surfaces caused by refraction of the OCT scanning beam.38 A single experienced operator performed all of the OCT scans and the biometric measurements using the OCT software. The same operator repeated the measurements at 1 week to test the intersession repeatability of the semimanual measuring procedure. Biometric measurements

were compared between the accommodation stimulus amplitudes using the Wilcoxon signed-rank test for pair comparisons and Friedman 2-way analysis of variance for multiple comparisons. Intersession repeatability was analyzed using the intraclass correlation coefficient (ICC) and the coefficient of repeatability (CoR) (1.96 multiplied by the SD of the differences between repeated measurements). The statistical analysis was performed using Excel software 2008 (Microsoft Corp.) and Statplus:mac 2009 software (Analystsoft Inc.).

RESULTS The study included 14 subjects (6 men and 8 women) with a mean age of 25.42 years G 8.21 (SD) (range 18 to 46 years). The mean uncorrected distance visual acuity (UDVA) was 0.043 G 0.05 logMAR, the mean uncorrected near visual acuity was 0.022 G 0.07 logMAR, and the mean refraction (mean spherical equivalent) was 0.25 G 0.25 D. Twelve subjects (all under 30 years old) completed the experiments at all amplitudes. One subject (aged 42 years) completed 3 of the experiments at amplitudes 0 D, 3.0 D, and 6.0 D. One subject (aged 46 years) completed 2 experiments at amplitudes 0 D and 3.0 D. Tables 1 and 2 and Figure 3 show the mean intraocular geometric distances obtained at each accommodation stimulus amplitude and their variations with accommodation. In addition to the measurements in Table 1, at amplitude 0 D, the mean CCT was 0.550 G 0.032 mm and the mean anterior chamber width was 11.975 G 0.419 mm. The lens thickness at amplitude 0 D showed a positive correlation with age (r Z 0.772, P ! .01). The CCT and anterior chamber width did not

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for ACD and r Z 0.724 for lens thickness. The anterior segment length did not change statistically significantly during accommodation (mean variation per diopter of 0.009 G 0.0085 mm; P Z .052), and the lens central point moved forward slightly with increasing amplitude (mean variation per diopter of 0.009 G 0.0080 mm; P ! .01) (Table 2 and Figure 3). Figure 4 plots the results of the analysis of lensthickness dynamics during accommodation (left) and disaccommodation (right) for cases 5, 9, 11, and 14. The intersession repeatability of the biometric measurements was excellent, with CCT, ACD, and lens thickness ICCs of 0.942, 0.998, and 0.991, respectively, and CoRs of 0.026, 0.035, and 0.057 mm, respectively.

Figure 2. Example of swept-source AS-OCT dynamic analysis of the crystalline lens shape changes during accommodation. A: The initial frame from Video 1, a vertical B-scan of accommodation in an eye included into the study. The lens is in the relaxed state (accommodation stimulus amplitude of 0 D). B: The initial frame from Video 2, a vertical B-scan of disaccommodation in a study eye. The eye is shown at the maximum accommodation stimulus amplitude of 9.0 D).

change statistically significantly with accommodation (P Z .064 and P Z .78, respectively). As the accommodation stimulus amplitude increased, there was a statistically significant decrease in the ACD (mean variation per diopter of 0.027 G 0.012 mm; P ! .05) and increase in the lens thickness (mean variation per diopter of 0.036 G 0.013 mm; P ! .001). The variations in ACD and in lens thickness were proportional to the change in stimulus magnitude (P ! .0001), with r Z 0.804

DISCUSSION Accommodation occurs through changes in the shape and thickness of the crystalline lens.1,2 According to Helmholtz' theory and other experimental findings,1,2 during near vision these changes are induced by the contraction of the ciliary muscle, which causes the release of the zonular fibers anchored to the equator of the crystalline lens. The thickness and the curvature of the lens increase, causing an increase in the eye's refractive power. Because it is a muscle-induced activity, accommodation is a highly fluctuant and dynamic process.2 Time-domain OCT has been used to perform biometry of the anterior segment at different static degrees of accommodation and in eyes of patients of different ages14,20,24,26,28–30 using low image resolution and limited axial range. The imaging speed of timedomain OCT systems is relatively slow, which precludes using it for dynamic imaging of accommodation. The more recent Fourier-domain OCT technology, including spectral-domain OCT (SD-OCT) and sweptsource OCT implementations, provides high axial resolution and the high imaging rate necessary for dynamic analysis of accommodation.12,13,15–17,23,25,36 The main limitations of commercial Fourier-domain OCT implementations are the relatively short axial range and the sensitivity decay with depth, which prevent simultaneous visualization of all the optical components of the anterior segment in a single

Table 1. Intraocular distances at different accommodation stimulus amplitudes. Mean Distance (mm) G SD Amplitude (D)

Anterior Chamber Depth

Lens Thickness

Lens Central Point

Anterior Segment Length

0 3.0 6.0 9.0

3.031 G 0.206 3.050 G 0.216 2.944 G 0.204 2.883 G 0.202

3.544 G 0.254 3.616 G 0.251 3.755 G 0.227 3.857 G 0.191

5.435 G 0.186 5.408 G 0.181 5.373 G 0.187 5.367 G 0.212

7.207 G 0.221 7.216 G 0.214 7.250 G 0.224 7.295 G 0.253

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Table 2. Mean variations in change to intraocular distances through different accommodation stimulus amplitudes. Amplitude (D) Measurement

†

Anterior chamber depth Lens thickness Lens central point Anterior segment length

3.0 0.063 G 0.045 0.072 G 0.059 0.027 G 0.021 0.009 G 0.024

6.0 0.187 G 0.068 0.239 G 0.082 0.067 G 0.032 0.053 G 0.029

9.0 0.263 G 0.086 0.385 G 0.074 0.071 G 0.081 0.122 G 0.091

P Value* !.001 !.001 !.001 .052

*Friedman 2-way analysis of variance for multiple comparisons † Values given as mean variation in change (mm) G SD

frame. In the past few years, an effort has been made to increase the imaging depth range and improve the sensitivity performance of Fourier-domain OCT systems. Imaging of the entire anterior segment along its whole depth has been obtained using experimental SD-OCT devices that use complex phase-splitting techniques for conjugate removal39,40; dual-channel, dualfocus SD-OCT devices25; and a technique of merging OCT images consecutively acquired at different depths using spectral domain implementations that have switchable reference arms.12,15,36 Swept-source OCT with a long imaging range (w12.0 mm in air) has been performed using high-speed reflective FabryPerot tunable lasers with a long coherence length that enables entire anterior segment imaging without the need for complex conjugate removal or reference-arm switching.13,23 A microelectromechanical-tuneable vertical-cavity surface-emitting laser light source was developed recently for swept-source OCT imaging at ultrahigh imaging rates (60 kHz to 1 MHz) and with a very long coherence length (w50 mm) that enables imaging of the entire eye.41 This advanced swept-source OCT implementation could offer significant advantages over previous systems used for dynamic imaging of the anterior segment but to our knowledge, a study of dynamic accommodation using this technology has not been reported. In the present study, an unmodified commercially available swept-source AS-OCT clinical device was used for imaging and performing biometry of dynamic accommodation. Despite the insufficient scan depth of the device (9.24 mm in air), simultaneous imaging of all anterior segment surfaces was achieved by acquiring OCT scans that overlapped the real and the conjugate images (Figure 1). No modifications to the hardware or software of the swept-source AS-OCT were necessary to image and obtain intraocular distances of the anterior segment at different accommodative states. The main limitation of this approach is that the internal structures of the crystalline lens cannot be clearly

distinguished and measured because of the overlapping of the real and conjugate images of the lens. Another limitation is that the posterior part of the crystalline lens is shown vertically inverted and displaced along the z-axis, so that the software provided with the clinical system cannot be used to correct for distortion in the images caused by refraction of the OCT beam at the different ocular boundaries. Hence, corrected nonaxial measurements such as curvature measurements or lateral distances could not be performed posterior to the anterior surface of the lens. A relatively simple solution to correct for full image distortion could be to develop custom software for boundary segmentation of the cornea and the lens that repositions the posterior surface of the lens with a vertical flip around the zero delay line and then performs distortion correction of the segmented boundaries using a ray-tracing algorithm based on Snell's law.38 In this case, the raw images would have to be exported to allow post-processing segmentation and correction of the ocular boundaries. To extract intraocular geometric distances, we used the refractive indices of the cornea and the aqueous provided by the swept-source AS-OCT quantification software. No equivalent refractive index for the crystalline lens was specified by the manufacturer. To our knowledge, an equivalent refractive index of the crystalline lens has not been reported for wavelengths of approximately 1300 nm. To extract the geometric thickness of the crystalline lens, we assumed an average refractive index of 1.421, a calculation from a previous study of OCT operating at 835 nm.37 As a consequence, all the lens-thickness measurements reported here might be affected by a minor constant scaling factor. Moreover, minor changes in the average index of the lens could occur during accommodation because of modifications in the gradient of the refractive index of the lens.42 The swept-source AS-OCT device used in our study has an active eye tracker for automated centering of the OCT images that increases the accuracy of the measurements. Previous studies using the same

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Figure 3. Intraocular distance changes during accommodation. The graph reports the mean axial distances of the corneal endothelium, lens anterior surface, lens central point, and lens posterior surface from the corneal epithelium for accommodation stimulus amplitudes 0, 3.0, 6.0, and 9.0 D.

swept-source AS-OCT device for biometric analysis of the anterior segment showed very high repeatability.31,32 In the present study, intrasession repeatability of the measurements was not assessed. However, manual measurements performed 1 week after the experiments using the swept-source AS-OCT device software showed good intersession repeatability. The results in the present study are in accordance with the model of accommodation previously proposed.1,2,43 The biometric analysis showed that the lens thickness increased and the ACD decreased with accommodation. Moreover, from biometry performed at different steps of accommodation, we found the variations in lens thickness and ACD to be proportional to the accommodation stimulus amplitude. In the present study, the anterior segment length (measured from the cornea to the posterior surface of the lens) showed a slight mean increase at the accommodated states, but the variation was not statistically significant. There is some controversy in the literature about the presence of an axial movement of the posterior surface of the lens during accommodation. Some studies showed no movement of the posterior surface of the lens and no variations of anterior segment length,19 whereas other studies showed a significant increase in anterior segment length at the accommodated states.36,44 This controversial topic is complicated by the variability of the average refractive index of the lens with lens-shape changes, which biases the measurements of anterior segment length during accommodation.42 The frame rate achieved by the OCT system (8 frames per second) was sufficient to detect the transient response to an accommodation stimulus change and to observe the evolution of the lens shape dynamically. However, a higher scan rate would be desirable to obtain a more accurate dynamic analysis of the lens to detect the continuous and rapid fluctuations associated with the accommodation process.45,46 In the case of an 18-year-old participant, the dynamic analysis of accommodation and disaccommodation showed that at the end of the disaccommodation sequence, the lens became thinner than it was before the accommodation sequence started (Figure 4, case 9). We cannot document a definite explanation for this result, but this behavior probably is related to the eye returning with disaccommodation to an accommodative state that is more relaxed than before the accommodation sequence commenced, when the so-called instrument myopia was probably occurring; this is especially likely considering the young age of the subject.47 Moreover, it has been described that the initial step destination of disaccommodative step responses tends to correspond to the cycloplegic refractive state.48,49

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Figure 4. Dynamic biometry of accommodation for 4 subjects of different ages. Changes in the lens thickness during accommodation are plotted as a function of time. The dynamic changes of the lens thickness are reported after the stimulus onset (at 0 seconds). The left graphs show the accommodation process from amplitude 0 D to 9.0 D. The right graphs show disaccommodation from 9.0 D to 0 D.

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A limitation of the present study is the absence of an objective measurement of the accommodation response. Measuring the power of the eye simultaneously with the OCT analysis (eg, using an autorefractometer) might increase the reliability of the measurements and could give useful information about the relationship between the changes in the shape and position of the lens and the power of the eye. In conclusion, OCT appears to be the most promising technology for studying accommodation in vivo. The study showed that high-resolution real-time imaging and biometry of the accommodating anterior segment can be effectively performed using a commercially available clinical instrument based on swept-source AS-OCT. This OCT system is a promising tool for studying the accommodation process in phakic and pseudophakic eyes implanted with accommodating intraocular lenses and could improve our understanding of the natural accommodative process and of the existing strategies for restoring accommodation. WHAT WAS KNOWN  An effective real-time imaging system to visualize the eye during accommodation is needed to improve the understanding of the mechanisms that govern normal accommodation and that cause presbyopia and set foundations for new procedures and implants to restore dynamic accommodation in presbyopic and pseudophakic eyes.  Fourier-domain OCT is the most promising technology for the study of the accommodation process in vivo. Major technical limitations (eg, limited imaging depth and the decay of sensitivity with depth) have not allowed visualization of the entire anterior segment in the study of the accommodation process. WHAT THIS PAPER ADDS  All of the anterior segment surfaces could be imaged simultaneously using a commercially available, sweptsource AS-OCT device, despite the device’s insufficient scan depth, by acquiring scans showing both the real and the conjugate images.  High-resolution dynamic imaging and biometry of the accommodating anterior segment could be effectively performed using a swept-source AS-OCT device. This OCT system could become useful for studying the accommodation process in phakic and pseudophakic eyes with accommodating intraocular lenses.

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First author: Alberto Neri, MD Ophthalmology Department, University of Parma, Parma, Italy