Low-Vision Rehabilitation with Audio-Biofeedback in Age-Related Macular Degeneration

Abstract

Audio-biofeedback (AFBF) with microperimetry is an important step in low-vision rehabilitation in age-related macular degeneration (AMD). After identifying the preferential retinal locus (PRL) with microperimetry, it is possible to begin rehabilitation to stabilize the PRL, increasing the quality of vision with 10 sessions of audio-biofeedback, at least one session per week, of 10 minutes for each eye. This involves presenting a chessboard grid in the site of fixation variable from the beginning to the end of the session. Audio-biofeedback allows for shifting the site of fixation to another point if the spontaneous fixation that the patient has found is not good to continue rehabilitation; at the end of biofeedback, we call this site the trained retinal locus (TRL) to differentiate it from the PRL. With audio-biofeedback, the low-vision patient with AMD acquires awareness about the best site of vision, thus improving the quality of vision, including better contrast sensitivity, visual acuity, color perception, and definition of the surrounding world.

1. Introduction

Age-related macular degeneration (AMD) is the primary cause of low vision in the Western world. Patients with low vision typically request treatment so that they can read, write, perform work, recognize faces, watch TV, drive a car, and so on. The damage induced by AMD leads to a central absolute or relative scotoma of different shape and extension, with subsequent loss or reduction of fine visual abilities like reading. Visual rehabilitation in AMD must begin with highlighting the vision needs of the patient. In most cases, being able to read is the first requirement. Face recognition is also very important, particularly when the visually impaired person is greeted by someone they cannot recognize, which may cause embarrassment and potential depression. The recovery of vision in intermediate visual activities such as writing, using the computer, and fine manual work are also fundamental, as is vision for watching television and movies.

The first step in visual rehabilitation is evaluating the patient’s residual vision for far and near, which can be unilateral or bilateral. This must be followed by determining the preferential retinal locus (PRL), which can be located above the macula atrophy, nasally, temporally, or inferiorly. The choice of mono or binocular optical aids for reading and distance vision is linked to the location of the PRL and the extent of the scotoma and the residual retina. It is essential to perform a series of orthoptic training for the localization and development of eccentric fixation, until the visually impaired patient becomes aware of their recovery abilities, being able to direct their gaze to the healthy retinal locus corresponding to the PRL. It is a long path that varies according to the depth of the low vision and the depth of the scotoma.

2. Audio-biofeedback

Audio-biofeedback (ABFB) is a process through which the subject learns and regains the ability to control and influence their own physiological responses through one psycho-physiological feedback and greater proprioception [1]. Biofeedback is used in rehabilitation and is based on biomechanical and physiological measurements of the body such as the neuromuscular, respiratory, and cardiovascular systems, movements, postural control, and force. An example of physiological biofeedback is electromyography biofeedback to increase the activity in weak or paretic muscles or to reduce the tone in spastic muscles. In electromyography, surface electrodes are used to detect a change in skeletal muscle activity, which is then fed back to the user by a visual or auditory signal. Another example is cardiovascular biofeedback, which is used to reduce blood pressure in hypertension and lower the mean heart rate [2].

In ophthalmology, audio-biofeedback is used in low-vision rehabilitation of maculopathy [3]. In our study, patients received eight monocular training sessions of audio-biofeedback, each lasting 10 minutes, every 7 days. Microperimetry (MP-1, Nidek Tech., Padova, Italy) was performed at the beginning and at the end of thesequence, as well as ETDRS visual acuity (VA) at 4 meters and Pelli-Robson Contrast Sensitivity (CS) at 1 meter.

Audio-biofeedback employs a sound to train the patient to keep a specific gaze position, which is marked on the digital retinal image by the operator and displayed as a target to the patient. If the patient’s gaze matches the selected position, a continuous sound is emitted. When the eye drifts away, the sound becomes progressively more discontinuous.

The contribution of audio-biofeedback to low-vision rehabilitation depends on the seriousness of the case, although it is useful in all cases. In some cases, where the PRL is in a good place, biofeedback allows stabilization of a fixation already used with the increase of retinal sensitivity in decibel and reduction of the fixation ellipse known as the bivariate contour ellipse area (BCEA).

In other cases, where the PRL used by the patient is in an area of little use for vision with an insufficient visual span to reading, audio-biofeedback allows shifting of the fixation to a better locus called the trained retinal locus (TRL).

2.1 Features and parameters of audio biofeedback

In audio-biofeedback with microperimetry, tracking is one of the key features, as it allows for automatic detecting of the patient’s eye movements during the exam of fixation as well as during the feedback training. The tracking detects and scores the patient’s fixation trajectory frame by frame. The user can preconfigure the parameters that define the characteristics of the fixation target, including the shape, extent, color, and thickness of the target.

There is the possibility to use letters or phrases as “custom” fixation.

The stability of fixation is classified [4, 5, 6] as follows:

1. Stable if more than 75% of the fixation points are contained within the circle with a diameter equal to 2°.

2. Relatively unstable if more than 75% of the fixation points are contained within the circle with a diameter of 2°.

3. Unstable if less than 75% of the fixation points are contained within the circle with a diameter of 4°.

The fixation itself is classified as follows:

1. Predominant central if more than 50% of the fixation points are contained within the foveal circle with a diameter of 2°.

2. Poorly central if the fixation points contained within the foveal circle are between 25% and 50%.

3. Predominantly eccentric if less than 25% of the fixation points are contained within the circle fixation trajectory.

The area of fixation is called bivariate contour ellipse area (BCEA) and is based on the published scientific literature [7]. The results of the relative analysis are converted into a graphical and numerical mode in three ellipses where the area and the measurements of each ellipse include different percentages of fixation points (68.2%, 95.4%, and 99.6%) corresponding respectively to 1–2-3 standard deviations. The BCEA is expressed in square degrees, the major and minor axes are expressed in degrees, and the inclination of the major axis is expressed from −90° to 90° with 0° for the horizontal position.

The normal value of BCEA is 0.5–1° squared.

In audio-biofeedback, the pattern used for rehabilitation training is a chessboard format with six alternating schemes with varying radius, frequency in Hertz (number of pattern image changes in each second), and degrees of retinal coverage from 2° to 8° with elements of 0.5° in size or more.

Patients are trained to fix the new area of the retina by asking them to move their gaze toward the new fixation. As the patient moves, an intermittent sound plays. The closer the patient gets to the new zone, the more the sound will be continuous.

2.2 Case 1

A 73-year-old woman presented with neovascular AMD treated with intravitreal anti-vascular endothelial growth factor therapy (anti-VEGF) in both eyes.

Best corrected visual acuity (BCVA) in the right eye was 20/400, and BCVA in the left eye was 20/500.

Microperimetry MP1 Nidek showed a spontaneous and unstable PRL localized below compared to atrophic fovea with a medium sensitivity of 8 dB in the right eye(Figure 1). The eccentricity of fixation measured by microperimetry was 4° (Figure 2). The PRL area represented by the BCEA was 111.28° squared (3 Std Dev) (Figure 3).

Figure 1.

Microperimetry before rehabilitation.

Figure 2.

Decentering of fixation before audio-biofeedback.

Figure 3.

BCEA before audio-biofeedback.

The left eye with a worse visual functioning situation showed a spontaneous PRL located below and nasally with a medium sensitivity of 7 dB (Figure 4).

Figure 4.

PRL and mean sensitivity.

The eccentricity of fixation was 6° (Figure 5) and BCEA was 71.89° squared (Figure 6).

Figure 5.

Decentralization of fixation.

Figure 6.

BCEA before audio-bofeedback.

The patient completed 10 sessions of audio-biofeedback lasting 10 minutes per eye. After the audio-biofeedback, there was an improvement in the quality of vision.

The best corrected visual acuity (BCVA) in the right eye improved from 20/400 to 20/200, and in the left eye it improved from 20/500 to 20/400. The contrast sensitivity and the parameters of microperimetry improved as well. In the right eye, the PRL shifted from below to the temporal position with an increase of mean sensitivity from 8 dB to 13 dB (Figure 7).

Figure 7.

In the RE the PRL shifted from below in temporal position.

The BCEA (bivariate contour ellipse area) decreased from 111.28° squared (3 st SD) to 31.12° squared, thus showing a clear improvement of fixation stability that is closely related to the improvement in mean sensitivity and to the shift of the PRL (Figure 8).

Figure 8.

Reduction of BCEA after ABFB with an increase in stability of the fixation.

Beyond improvement in visual acuity, contrast sensitivity, stability of fixation, and sensitivity, as well as relocated fixation, the patient acquired the awareness of his own ability to fix, to use the visual residual, and to move toward the best site of vision (Figure 9).

Figure 9.

The ocular movement toward the best eccentric fixation area allows the visually impaired patient with maculopathy to be able to see the tree.

2.3 Case 2

A 68-year-old woman presented with atrophic AMD. BCVA in both the right eye and left eye was 20/400.

The first microperimetry showed a central scotoma with a sensitivity of 0 dB without presence of PRL in the right eye but of an erratic searching of the presented fixation point without a precise point of fixation (Figure 10).

Figure 10.

RE: Erratic fixation.

The BCEA area was 314.87° squared, and it was not possible to find the decentralization of fixation for the absence of fixation (Figure 11).

Figure 11.

RE: BCEA 314.87° squared.

Microperimetry showed an unstable and spontaneous PRL located below the atrophic fovea with a mean sensitivity of 8 dB in the left eye (Figure 12).

Figure 12.

Unstable and spontaneous PRL located below the atrophic fovea.

The BCEA in the left eye was 90.10° squared (Figure 13).

Figure 13.

BCEA 90.10° squared.

The decentralization of fixation compared to the atrophic fovea was 7° (Figure 14).

Figure 14.

Decentralization of eccentric fixation of 7°.

The patient completed 10 sessions of audio-biofeedback in both eyes.

The purpose of the audio-biofeedback was to move the fixation up. In the right eye with erratic fixation, the cross was placed above the atrophic fovea, instead in the left eye the cross was placed above compared to the spontaneous PRL, which was located below the atrophic fovea (Figure 15). The passage from erratic fixation to superior fixation occurred gradually (Figure 16).

Figure 15.

Positioning of the best eccentric fixation in both eyes above the atrophic fovea.

Figure 16.

Gradual shifting of fixation toward the best site of vision.

In the right eye, the fixation was shifted above and the sensitivity increased from 0 dB in the initial central scotoma with erratic fixation to 10 dB of mean sensitivity with the formation of a new area of fixation called the trained retinal locus (TRL) (Figure 17).

Figure 17.

RE: In the new trained fixation (TRL), the sensitivity is 10 dB.

The BCEA in the new fixation, named TRL, was 144.24° squared (Figure 18) against 314.87° squared before the audio-biofeedback.

Figure 18.

RE: BCEA (bivariate contour ellipse area) after audio-biofeedback.

After ABFB, the visual acuity improved to 20/200 in both eyes and contrast sensitivity on the Pelli Robson chart increased from 0.60 to 0.90.

2.4 Case 3

A 67-year-old woman presented with AMD. Visual acuity in the right eye was finger count of 20 cm. Visual acuity in the left eye was 20/400 with visual disability. The patient was unable to read and cannot see faces. She was also unable to walk alone without serious problems in orientation and mobility.

Microperimetry showed an erratic fixation without a precise localization with central absolute scotoma and a sensitivity of 0.1 dB (Figure 19).

Figure 19.

RE: Erratic fixation.

BCEA in the right eye was 185.08° squared in an erratic fixation (Figure 20).

Figure 20.

RE: BCEA 185.08° squared in erratic fixation.

In the left eye, there was a central absolute scotoma with a sensitivity of 0.00 dB (Figure 21).

Figure 21.

LE: Absolute central scotoma.

BCEA in the left eye was 192.82° squared (Figure 22).

Figure 22.

LE: BCEA 192.82° squared.

After 10 sessions of audio-biofeedback, we obtained a shift of the erratic fixation in a new PRL, named TRL, localized inferiorly to the optic disk near the very large atrophic maculopathy, extended beyond the posterior pole, with a sensitivity of 0.7 dB instead of 0.1 dB at the start. The sensitivity of the retina in the new area of fixation reached a good value of intensity until 10 dB (Figure 23).

Figure 23.

RE: Trained retinal locus localized inferiorly to the optic disk with a sensitivity of 0.7 dB instead of 0.1 dB before audio-biofeedback in the erratic fixation.

In the new area of fixation, the BCEA was 73.39° squared (Figure 24).

Figure 24.

RE: BCEA 73.39° squared instead 185.08° squared before audio-biofeedback.

In the left eye, after audio-biofeedback, we obtained a new area of fixation in the same site of the right eye, below the optic disk and near the large atrophic macular degeneration with a sensitivity of 0.5 dB from the initial absence in the central absolute scotoma (Figure 25).

Figure 25.

LE: Trained retinal locus localized below the optic disk.

The BCEA of the new TRL was 99.6° squared (Figure 26).

Figure 26.

In the new trained eccentric fixation, the BCEA decreased from 192.82° squared to 99.6° squared.

Visual acuity in the right eye improved from finger count to 20/400. Visual acuity in the left eye improved from 20/400 to 20/250. Before rehabilitation, the patient was not able to read with electronic aid. After ABFB, she was able to read with CCTV. Furthermore, she was able to see more clearly when walking, see the number of days of months in the calendar without glasses, and look at photos of family members. When she was able to see her father’s photo, she was moved!

Often in low-vision rehabilitation, we find a PRL localized very far from the atrophic fovea (Figures 27 and 28).

Figure 27.

Atrophic AMD with PRL located up in both eyes and very far from atrophic fovea.

Figure 28.

Atrophic AMD with PRL located down in both eyes and very far from atrophic fovea.

In other cases, the PRL may be closer to the atrophic fibrotic fovea (Figure 29).

Figure 29.

PRL located up from atrophic fovea.

Still, in other cases, a very unstable foveal fixation must be stabilized (Figure 30).

Figure 30.

Stabilization of fixation.

In this case, we used a custom target of fixation with a four-word phrase that the patient can read when presented in the best area of fixation.

Figures 31 and 32 are examples of chessboard patterns used for audio-biofeedback.

Figure 31.

Example of chessboard pattern used for audio-biofeedback.

Figure 32.

Example of chessboard pattern used for audio-biofeedback.

Audio-biofeedback may be applied in other types of maculopathies such as hereditary retinal dystrophy, Stargardt disease, cone dystrophy, Best maculopathy, and myopic degeneration (Figures 33–36).

Figure 33.

Stargardt disease before audio-biofeedback.

Figure 34.

Microperimetry in Stargardt disease after audio-biofeedback.

Figure 35.

Microperimetry in best disease after audio-biofeedback.

Figure 36.

Myopic macular degeneration.

3. Conclusions

The improvements of retinal sensitivity in the new area of fixation (TRL) go hand in hand with an improvement in the quality of vision and the quality of life. Before low-vision rehabilitation with audio-biofeedback, the visually impaired patient is submitted to the Italian version of the Veterans Affairs (VA) Low-Vision Visual Functioning Questionnaire (LV VFQ-48) [8] based on the idea of Stelmack JA et al. [9] and with the permission of the authors. LV VFQ-48 is a fundamental instrument for measuring the difficulty low-vision persons have in performing daily activities and evaluating vision rehabilitation outcomes.

After rehabilitation with audio-biofeedback, there was a positive change in the score regarding better vision in activities of daily living.

The chessboard pattern has an alternating reversal presentation. This leads to a neuro-visual stimulation of retina cells and consequently to a stimulation of the visual cortex with a cerebral reorganization based on the new occipital projection of the new PRL, which replaces the nonfunctioning macula [10, 11].

In conclusion, audio-biofeedback can stabilize the PRL with increased retinal sensitivity and improvement in BCEA, represented by a decrease in the fixation area. It can also lead to the development of a new area of fixation called the trained retinal locus (TRL).

Audio-biofeedback contributes to the patient’s awareness of “where to look to see better.” As such, ABFB for low-vision rehabilitation can improve both the quality of vision and the quality of life.