Electroretinogram (ERG) is the only clinical objective test available to assess retinal function. Full-field ERG (ffERG) measures the panretinal rod and cone photoreceptor function as well as inner retinal function and is an important measure in the diagnosis and management of inherited retinal diseases as well as inflammatory, toxic, and nutritional retinopathies. Adhering to international standards and maintaining retinal dark adaptation are critical to acquire valid and reliable dark-adapted (scotopic) and light-adapted (photopic) ffERG responses. Performing ffERG in infants and children is challenging and often requires general anesthesia in the operating room. However, maintaining retinal dark adaptation in the operating room is becoming increasingly difficult given the numerous light sources from anesthesiology monitoring systems and other equipment. A practical and widely applicable method for ffERG testing is described in the operating room that optimizes retinal dark adaptation. The method reduces operating room time by dark-adapting the patient before general anesthesiology is instituted. The operating room is modified for dark adaptation and any remaining light source in the darkened operating room is minimized with the use of a modified portable foldable darkroom that encloses the patient’s head and the ERG examiner during ffERG scotopic recordings. The simple method adheres to ffERG international standards and provides valid reliable scotopic and photopic ffERG recordings that are critical to assess objective retinal function in this young age group where subjective assessment of visual function such as visual acuity and visual fields are not possible. Furthermore, the ffERG is the gold standard clinical test in detecting early onset inherited retinal diseases including Leber congenital amaurosis where approved gene therapy has become available. In sedated conditions, very low amplitude ffERG signals can be detected due to minimal orbicularis muscle activity interference, which is particularly relevant in patients after gene therapy to detect improved amplitude responses.
The electroretinogram (ERG) is the only clinical objective test available to assess retinal function and the full-field ERG (ffERG) is the only objective test to assess rod-photoreceptor generated activities1,2. The ffERG measures the electrical responses from the entire retina elicited by a full-field flash stimulus and is a gold standard test in the diagnosis and management of inherited retinal diseases2,3. Thus, the ffERG is an important test in infants and young children to detect early onset inherited retinal diseases such as Leber congenital amaurosis where approved gene therapy and clinical trials are available4,5.
Adherence to ffERG standards established by the International Society for Clinical Electrophysiology of Vision (ISCEV) are critical to acquire valid and reliable dark-adapted (scotopic) and light-adapted (photopic) ffERG responses1,3. Failure to properly maintain adequate retinal dark adaptation during scotopic ffERG recordings results in falsely-impaired recorded responses and patient mismanagement. Performing ffERG in infants and children is challenging given limited cooperation and often requires general anesthesia in the operating room6. A recent survey among ISCEV members showed 12-14% of ERG’s are performed under sedation or general anesthesia7. Maintaining retinal dark adaptation in the operating room is difficult given the numerous light sources from anesthesiology monitoring systems and other equipment. While anesthetic agents may have an effect in reducing ERG responses, ERG responses under sedation or general anesthesia are reliable in providing accurate diagnosis6,8,9.
A simple and widely applicable method is described for ffERG testing in the operating room that adheres to the international standards and optimizes retinal dark adaptation. The goal of this practical method is to provide valid reliable scotopic and photopic ffERG recordings to assess objective retinal function in infants and young children, which is particularly relevant in this young age group given subjective assessment of visual function such as visual acuity and visual fields are typically not possible. The operating room is modified to promote retinal dark adaptation, and the procedures reduce operating room time by dark-adapting the patient before sedation or general anesthesiology is instituted. A modified portable foldable darkroom encloses the patient’s head and the ERG examiner during ffERG scotopic recordings to minimize any remaining light source including light emission from the ERG system. The portable darkroom allows rapid access to the patient by the anesthesiologist when necessary. After the completion of ffERG, diagnostic retinal imaging including optical coherence tomography (OCT) and fundus imaging as well as venopuncture for genetic testing can easily be performed while the patient remains under anesthesia.
The method is suitable for practitioners and practices that manage pediatric patients with retinopathies. An average sized ocular operating room provides adequate space, and a room with low background electrical noise is desirable to allow quality ffERG recording. While the ERG examiner is inside the foldable darkroom during scotopic ffERG recording, a trained technician is needed to operate the ERG system outside of the foldable darkroom. Conferring with the anesthesiology team is essential in modifying the operating room and to promote the safety of the patient in a darkened environment.
The advantages of the method over alternative techniques include optimizing and maintaining retinal dark adaptation, promoting valid reliable ffERG recordings, improving patient safety, and facilitating additional diagnostic testing such as retinal imaging and venopuncture for genetic testing. Optimal dark adaptation is also critical given ffERG stimulators should be calibrated for complete darkness conditions as recommended by ISCEV10. Alternative methods include the use of oral agents such as chloral hydrate with variable sedative responses in infants and children, which affects the quality of ffERG recordings and causes difficulties in monitoring vital signs. While some children can cooperate with ffERG recording in the clinic, the testing session may be prolonged depending on cooperation, and the validity of ffERG recordings may be affected by eye movement and blink artifacts as well as difficulty in maintainng retinal dark adaptation4. The current method provides additional dark adaptation and safety measures compared to the previously described deep sedation ffERG method6.
The protocol follows the operating room guidelines of the Bascom Palmer Eye Institute, University of Miami and is applicable to infants, young children, and uncooperative adults. Patients who cannot have general anesthesia due to safety issues should not have the procedure.
1. Operating room selection and modification
- Select an operating room with low 60 Hz background electric current noise and proper electrical grounding, to avoid ERG recording interference. Use a room with an isolated electrical circuit without connection to or is near heavy appliances (e.g., refrigerator).
- Perform trial ERG recordings in the operating room at the location where the ERG recording will take place. Check the ERG recording baseline as well as the trial recording waveforms to determine the absence of 60 Hz background electric noise.
- Inspect the operating room for light leaks from ceiling, door, and window openings. Perform human observation after full dark adaptation (30 to 45 minutes) given that the normal human eye can detect light as dim as approximately 4 photons, which is better than any man-made light meter except liquid nitrogen-cooled detectors for astronomy.
- Install opaque non-reflective black curtains on tracks to cover the operating room door and window openings fully without light leakage (Figure 1). Select curtain material that is washable and resistant to staining and bacterial growth. Follow local operating room regulations and procedures for proper interval cleaning. Block light leaks from the ceiling if present.
2. Foldable portable darkroom selection and modification
- Select a portable darkroom that is easy to install and store and large enough to enclose the patient’s head, the ERG examiner, and the ffERG stimulus. Use folding portable darkrooms designed for an optic physicist (e.g., www.scientex.co.jp/pdf/pdf-b-lp-eng.pdf, 48”x 48”x81” cross type) which are available commercially and optimizes the maintenance of retinal dark adaptation of the patient during scotopic ffERG recordings (Figure 2).
NOTE: The fabric of the portable darkroom mentioned was tested by the eye institute’s microbiology department for ease of disinfection and the optical transmission was tested by the eye institute’s biomedical department before purchase. This is recommended if a different portable darkroom is used.
- Add a small opening with double flaps at the rear of the portable darkroom to allow routing connections and cables (Figure 3).
NOTE: During scotopic ffERG testing, the ffERG light stimulus is inside the folding portable darkroom and the ERG recording system is outside of the portable darkroom. The ERG electrode wire connections and the cable connecting the ERG light stimulus to the ERG recording system go through the opening created with a double closure system to ensure total darkness. We use a small handheld ffERG light stimulus to ease ERG recording inside the folding portable darkroom and record one eye at a time. A larger ffERG light stimulus can record both eyes simultaneous but will need to be held by a metallic arm requiring a larger opening at the rear of the portable darkroom and will likely require a larger darkroom.
3. Patient preparation and retinal dark adaption
- Confirm medical reason for ffERG and obtain informed consent for examination under anesthesia, ffERG, and other procedures of interest for patient management such as retinal imaging (e.g., fundus imaging, optical coherence tomography, fluorescein angiography) and venopuncture for genetic testing.
NOTE: Most common reasons for ffERG in infants and young children include decreased vision, nystagmus, nyctalopia, visual photosensitivity, abnormal fundus, and medication with risk of retinal toxicity (e.g., vigabatrin). Important to recognize factors that are likely to affect ERG recordings including high myopia and albinism. In general, ffERG responses from infants younger than age 6 months are small and still developing, making interpretation of recorded responses difficult.
- Place ocular anesthetic drop (proparacaine 0.5%) followed by pupillary dilation combo drop (cyclopentolate 1% + phenylnephreine 0.5%) to each eye. Repeat the combo drop to each eye 2 to 3 times with 5 minutes between drops.
NOTE: The proparacaine decreases burning sensation and increases corneal absorption of the dilating drops but may have to be skipped in patients with very poor cooperation.
- Patch both eyes for retinal dark adaptation of at least 30 minutes. With eyelids gently and completely closed, place 2 regular-size self-adhesive eye occlusion patches over each eye without significant pressure on the eye.
- Place the first patch conventionally and oriented horizontally with the wider end of the patch temporally. Place the second patch horizontally over the first patch with the wider end nasally and adjust the position typically with a tilt counterclockwise to prevent light leak nasally.
- After placing the eye patches over each eye, place opaque black tape horizontally across to cover both eyes without significant pressure on the eyes. Make a small vertical cut at the inferior edge of the black tape before placement at the location across the bridge of the nose to avoid pressure on the nose.
- Place the black opaque relaxation sleeping mask with head headband over the patched eyes (Figure 4).
NOTE: ISCEV international standard for dark adaptation is 20 minutes. Dark adaptation of at least 30 minutes is preferred to facilitate optimal scotopic ffERG recording given the retinal dark adaptation curve reaches a more asymptotic point compared to 20 minutes. Based on our experience, vast majority of infant and young children are tolerant of bilateral patching, and parental support and encouragement are critical. Explaining the purpose of dark adaptation and the benefit of reducing general anesthesia time helps the parents to understand. Parental tender loving care including cuddling, music from cell phone, and pacifier are very helpful during the dark adaptation period. Of over 120 infants and young children who underwent the method, only 2 patients could not tolerate bilateral patching for dark adaptation. Both patients were dark-adapted after general anesthesia induction instead and the ERG responses were subsequently successfully recorded using the same method.
4. Dark-Adapted full-field electroretinogram recording in the operating room
- Prepare the operating room by placing translucent red filter films over monitors and opaque black tape over LEDs and light sources (Figure 5A-5B). Set up folding portable darkroom. Close curtains over door and window openings.
- Induce general anesthesia or sedation by anesthesiology team on bilaterally-patched patient followed by continued anesthesiology monitoring. Perform timeout to verify procedures to be performed.
- Place ERG recording electrodes, ffERG light stimulus, a very dim red light mounted on a forehead band, topical 0.5% ophthalmic proparacaine, 2.5% ophthalmic hydroxypropyl methylcellulose (if Burian-Allen electrode is used), and sterile gauze (for wiping excess methylcellulose) close to ERG examiner position before placing the portable darkroom to enclose the head of the patient and ERG examiner (Figure 6A). The ERG examiner will be using the mounted red forehead band to perform scotopic ffERG recordings.
NOTE: The red light mounted on a forehead band is modified by placing layers of red light filter films over the LEDs. The red light should be as dim as possible to allow the ERG examiner to perform the procedure so dark adaptation is maintained. Helpful for the examiner to wait a few minutes to have some of his or her own partial dark adaptation before placing the electrodes. Experienced ERG examiners tend to use very dim red light or can do the procedure by feel without any red light if Burian-Allen electrode is used.
- Place the ground ERG electrode clip with conductive paste on one ear lobe. Snake the ground ERG electrode connection and ffERG light stimulus cable through the modified flap opening of the portable darkroom and the ERG technician connects them to the ERG system outside of the darkroom.
- Close the front opening of the portable darkroom with large binder clips. Turn off room lights and check and cover any remaining uncovered light sources with black tape.
- Remove the black mask over both eyes. Remove the black tape and patches over the right eye only and place the corneal ERG recording electrode on the right eye to record the scotopic ffERG responses using the hand-held full-field light stimulus in accordance to the ISCEV standards (Figure 6B).
- Snake the ERG recording electrode connection through the modified flap opening of the portable darkroom for the ERG technician to connect it to the ERG system outside of the darkroom. Take care to use the dimmest red light possible, and a brief period of additional dark adaptation, approximately 5 min, is recommended for recovery after lens insertion in accordance to the ISCEV standards.
- After checking for electrical baseline stability and ERG electrode impedance, proceed with recording of the rod responses (dark-adapted 0.01 cd·s·m-2 flash ERG), followed by the combined rod-cone responses (dark-adapted 3.0 cd·s·m-2 flash ERG and 10 cd·s·m-2 flash ERG) and the dark-adapted 3.0 flash oscillatory potential responses. Be mindful of the recommended time intervals between the light stimulus to maintain dark adaptation.
NOTE: When a handheld ERG light stimulus is used to test one eye at a time, keep the other eye monocular patched to maintain dark adaptation during scotopic recordings of the first eye. Dawson Trick Litzkow (DTL) fiber electrode or bipolar Burian-Allen ERG corneal electrodes are typically used. The DTL electrode is better tolerated by a conscious patient and has lower amplitude-to-noise ratio compared to the Burian-Allen ERG corneal electrode. Given patient tolerance is not an issue during sedation or general anesthesia, Burian-Allen electrode is preferred for sedated ERG recordings given its superior amplitude-to-noise ratio.
- Remove the black tape and patches of the left eye and proceed with scotopic ffERG recording of the left eye following same procedures as for the first eye as in step 4.6 with the hand-held full-field light stimulus.
NOTE: Recorded scotopic ffERG amplitudes tend to be mildly lower in the second recorded eye given the retinal dark adaptation of the second eye is typically affected by the ERG stimulus flashes diffusing to the eye through bone and tissue during ERG recording of the first eye.
5. Light-Adapted full-field electroretinogram recording in the operating room
- After completion of the scotopic ffERG recordings, turn on all overhead room lights. Disconnect the ERG electrode connections and the ffERG light stimulus cable from the ERG recording system and snake them back to the inside the portable dark room through the modified flap opening. Remove the portable dark room.
- Light adapt both eyes for 10 minutes by using the overhead room lights in accordance to the ISCEV standards (background luminance 30 cd·m-2). Keep the bipolar Burian-Allen ERG electrodes in place for both eyes given the built-in eyelid speculums of the electrodes will hold the eyes open. If DTL lenses are used, use eyelid speculums to keep both eyes open with instillation of periodic lubricating eye drops to avoid corneal drying.
- Connect the ERG electrode connections and the ffERG light stimulus cable to the ERG system and proceed to record, in accordance to the ISCEV standards, the cone flash responses (light-adapted 3.0 cd·s·m-2 flash ERG) followed by the cone flicker responses (light-adapted 3.0 flicker ERG).
NOTE: This completes the ffERG recording. Other diagnostic retinal imaging including OCT, fundus photos as well as venopuncture for genetic testing can easily follow while the patient remains sedated.
Using the method described, valid, reliable, interpretable normal and abnormal ffERG responses are feasibly obtained in the operating room for infants and young children under sedation or general anesthesia. In particular, falsely low scotopic ffERG responses are avoided, and common retinal causes of decreased vision and nystagmus in this age group are readily identified. For instance, the preservation of scotopic ffERG responses is important to differentiate Leber congenital amaurosis from achromatopsia where the cone ffERG responses are diminished in both conditions but the scotopic ffERG responses are preserved in achromatopsia but not in Leber congenital amaurosis (Figure 7). Obtaining good quality scotopic ffERG responses is also important to diagnose conditions where distinct scotopic ffERG waveform morphology is present. For example, the presence of a negative b-wave in the scotopic combined rod-cone ffERG response is a key feature of congenital stationary night blindness (Figure 7). While anesthetic agents may reduce ERG responses, ERG responses under anesthesia are reliable in providing accurate diagnosis.6 The lower limit of the normal range of the ERG responses is age dependent and increases with age. For instance, the lower limit of normal for age 12 months to 24 months for the scotopic rod responses with the Burian-Allen electrode is 75 µV. As recommended by ISCEV, individual ERG labs are encouraged to collect own normal values.
The method is used reliably to determine disease progression over time. For instance, the systemic features of Alström syndrome are subtle in very young patients and the initial ffERG responses may be similar to achromatopsia with relative preservation of scotopic ffERG responses and diminished cone responses (Figure 8). Over time, the scotopic ffERG responses worsen showing a cone-rod dysfunction pattern that is consistent with conditions including cone-rod dystrophy and secondary syndromic cone-rod degenerations such as Alström’s syndrome (Figure 8).
Figure 1: Dark proofing of openings of operating room. Opaque non-reflective black curtains cover operating room door and window openings. Please click here to view a larger version of this figure.
Figure 2B: Folding portable darkroom. Commercially available foldable portable darkroom (A) isolates the patient’s head and the ERG examiner (B) to optimize the maintenance of retinal dark adaptation during scotopic ffERG recordings (photo taken with lights on before starting case for illustration purposes). Please click here to view a larger version of this figure.
Figure 3C: Modification of the rear of the darkroom. Small opening created at the rear of the darkroom (A) covered by double flaps (B) allow routing connections and cables to the ERG recording system outside of the darkroom (C). Please click here to view a larger version of this figure.
Figure 4: Dark adaptation with bilateral patching. A dark relaxation mask is placed over the patient after each eye is patched by placing a layer of black tape over 2 eye pads over closed eyelids. Please click here to view a larger version of this figure.
Figure 5B: Dark proofing of operating room.
Translucent red filter films (A) are taped over monitors and opaque black tape (B) covers LEDs and light sources. Please click here to view a larger version of this figure.
Figure 6B: Recoding scotopic ffERG responses inside darkroom.
Patient with darkroom in place (A). Scotopic ffERG responses are recorded in a very darkened environment inside darkroom (B) with a very dim red light mounted on a forehead band used to place corneal ERG recording electrodes in place (photo taken with lights on before starting case for illustration purposes). Please click here to view a larger version of this figure.
Figure 7: Normal and abnormal ffERG examples. Standard ffERG responses obtained with method in infants and young children showing normal responses and valid reliable scotopic and photopic responses that easily differentiate Leber congenital amaurosis (LCA), achromatopsia, and congenital stationary night blindness (CSNB). LCA example is a 6-year-old with RDH12 genotype; achromatopsia example is a 3-year-old with PDE6C genotype; CSNB example is a 3-year-old with TRPM1 genotype. Please click here to view a larger version of this figure.
Figure 8: ffERG example showing disease progression. Standard ffERG responses obtained with method obtained in a 2-year-old patient with follow-up 2 years later. Progression of the scotopic ffERG responses is evident, and patient was found to have Alström syndrome. Please click here to view a larger version of this figure.
The methodology and protocol describe how to effectively perform valid and reliable ffERG in infants and children under sedation or general anesthesia in the operating room. The major concept and aim of the technique are to provide and maintain optimal retinal dark adaptation during scotopic ffERG recordings. This is essential to provide accurate objective assessment of rod photoreceptor function given retinal dark adaptation is rapidly diminished by exposure even to dim light leading to erroneous recorded responses. The critical steps of the method are (i) to choose an operating room with low 60 Hz background electric current noise, proper electrical grounding and to modify and prepare the room meticulously to block light sources (ii) to pharmacologically dilated the pupils fully and to place multi-layer eye patches that completely blocks light to induce retinal dark adaptation (iii) to use a modified portable foldable darkroom that encloses the patient’s head and the ERG examiner, and (iv) to use the least amount of dim red light needed inside the darkroom during scotopic ffERG recording.
The method is significantly superior to existing alternative methods. While performing ffERG without sedation in infants less than 1 year old may be possible by using a feeding bottle and some children can cooperate with ffERG recording, cooperation is poor in most infants and young children. Performing ffERG with oral sedation in a conventional ERG recording darkroom lacks the ability to monitor the patient’s cardiopulmonary function safely and the spectrum of responses to the oral sedation is wide and unpredictable. Performing ffERG in a darkened operating room without a portable darkroom is typically not dark enough to adequately achieve and maintain dark adaptation given the growing number of new anesthetic and operating room equipment.
The method works well with a small handheld ffERG light stimulus given the limited space inside the portable darkroom, and ffERG recording is done one eye at a time. A larger full-size full-field ERG stimulus dome will allow simultaneous ERG recording of both eyes and shorten examination time. A full-size ERG stimulus dome would require a metallic arm to hold it securely over the supine patient and a larger portable darkroom with a much larger flap opening would be required to accommodate the metallic arm. Such modification is possible with care to create a large flap opening that is not prone to light leak.
Limitations of the method are few and include the effect of sedative and general anesthetic agents in reducing ERG responses, which is not substantial enough to influence accurate clinical diagnosis and follow-up testing to assess progression. The method requires the cooperation of the pediatric anesthesiology team to monitor patient in a dimly lit operating room for 15 minutes during scotopic ffERG recording. If anesthetic emergency arises, the procedure can be aborted immediately and the portable darkroom can be moved rapidly to allow full patient access.
The authors have nothing to disclose.
This paper is supported in part by the James V. Bastek, M.D. Hereditary Retinal Disease Research Program, Bascom Palmer Eye Institute, University of Miami, FL, USA; NIH Center Core Grant P30EY014801; Research to Prevent Blindness Unrestricted Award and Career Development Awards; Florida Lions Eye Bank and the Beauty of Sight Foundation, Miami, FL, USA; and Henri and Flore Lesieur Foundation.
|Black tape||3M Industrial Adhesives and Tapes Division, St Paul, MN 55144-1000 USA||3M ID 70016070396|
|Conduction skin paste||Redux Electrolyte Paste, Hewlett Packard company, USA||67-05|
|Darkroom - Portable foldable||Scientex Inc., Japan||B-LP1/B-LP1-X||Requires modification as described in Protocol|
|Dark adaptation mask (relaxation sleeping mask)||Mindfold Inc, Durango, CO, USA||6576493||Flexible black plastic face plate backed with a high-density soft foam padding that allows total darkness.|
|Ear clip for electric grounding||Natus - Nicolet Neurodiagnostic, UK||F-E34DG-72||Grass 10mm Gold Cup EEG Ear Clip with touchproof connector 72" wire - Set of 2|
|Electrodes ERG recording (Burian-Allen, DTL)||Burian-Allen, Hansen Ophthalmic Develoment Lab, Iowa, USA; DTL, Diagnosys, Lowell, MA 01854, USA.||303-20LA, 303-20A, 303-20P, 303-20I, 303-20SI||Available in different sizes|
|ERG systems including handheld full-field stimulus||Any system meeting the standards established by the International Society for Clinical Electrophysiology of Vision (ISCEV).||Authors use Diagnosys and Roland systems; other ISCEV standard systems available.|
|Eye drops and Gel, proparacaine, phenylephrine, cyclopentolate, methylcellulose||Ophthalmic drops, Proparacaine 0.5%, phenylephrine 2.5%, cyclopentolate 1%, Akorn, Inc. Forest, IL 60045 USA; ophthalmic gel, methylcellulose 2.5%, Alcon Laboratory, Inc. Fort Worth, TX 76134 USA|
|Eye patch||BSN Medical Inc, Rutherford College, NC, USA||46430-00||Coverlet eye occlusor for treatment of lazy eye|
|Head band with light||REMIX PRO. Princeton Tec,
Trenton, NJ 08650 USA
|RMX300PRO-RD-BK||Requires placing layers of red filters over LED as described in protocol|
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