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Clinical Sciences |

Identifying Live Nematodes in Diffuse Unilateral Subacute Neuroretinitis by Using the Scanning Laser Ophthalmoscope FREE

Lúcio R. Moraes, MD; Arnaldo P. Cialdini, MD; Marcos P. Avila, MD, PhD; Ann E. Elsner, PhD
[+] Author Affiliations

From the Retina Ophthalmology Unit, Department of Ophthalmology, Centro Brasileiro de Cirurgia de Olhos and the Universidade Federal de Goiás, Goiânia, Brazil (Drs Moraes, Cialdini, and Avila); the Universidade Federal de São Paulo, São Paulo, Brazil (Dr Moraes); and the Schepens Eye Research Institute, Harvard Medical School, Boston, Mass (Dr Elsner). The authors have no commercial interest in the scanning laser ophthalmoscope, any hardware associated with it, or the software developed for it.


Arch Ophthalmol. 2002;120(2):135-138. doi:10.1001/archopht.120.2.135.
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Published online

Objective  To describe use of the scanning laser ophthalmoscope (SLO) to identify live nematodes in patients with diffuse unilateral subacute neuroretinitis.

Methods  Infrared, red, and blue illumination (780, 633, and 488 nm, respectively) in an SLO were used to image and evaluate functional retinal status in patients with late-stage diffuse unilateral subacute neuroretinitis. An examination to identify live nematodes was performed in the affected eyes.

Results  Using blue illumination, the ocular fundus appeared dark and provided a high-contrast background for the white image of the worm. The red laser was used to perform red-on-red perimetry. We also used perimetry stimulus to stimulate the worm's movement and pinpoint its location. We precisely defined the relation between the fixation point and the worm to plan accurate laser treatment. The infrared laser is safe and comfortable for prolonged examination. Using the SLO, several physicians simultaneously visualized the ocular fundus. Video output from the SLO provided temporal information, excellent for enhancing detection of worms, which was displayed dynamically on video.

Conclusions  Although examination with a fundus contact lens by skilled ophthalmologists is the method of choice, the SLO provides a new examination modality with distinct advantages for identifying live worms in young patients with diffuse unilateral subacute neuroretinitis.

Figures in this Article

DIFFUSE UNILATERAL subacute neuroretinitis (DUSN) is a clinical syndrome characterized in the early stage by visual loss, vitritis, papillitis, retinal vasculitis, and recurrent crops of evanescent gray-white outer retinal lesions and later by progressive visual loss, optic atrophy, retinal vessel narrowing, and diffuse retinal pigment epithelium (RPE) degeneration occurring in one eye of otherwise healthy patients.13 The first patient, to our knowledge, with documented bilateral nematodes was described recently.4 During the early course of the disease, visual acuity may be normal or minimally affected.1,5 In many patients, particularly in young children, the disease remains undetected until the visual acuity decrease is found during a school vision examination.

Diffuse unilateral subacute neuroretinitis is caused by at least 2 unidentified nematodes of different sizes that vary in length from 400 to 2000 µm.15 Cialdini et al6 recently reported the first South American case of DUSN caused by the larger nematode. The nematode can be found at any stage of the disease and should be sought in patients with optic atrophy, narrowing of the retinal vessels, and advanced degenerative RPE changes.5

A careful search using a fundus contact lens is required to locate smaller worms, which are barely visible by indirect ophthalmoscopy using a 20-diopter lens. Larger worms are relatively easy to detect using indirect ophthalmoscopy and are most likely found near active, deep, white retinal exudative lesions, which are probably caused by a toxic inflammatory reaction to material left in the wake of the nematode moving in the subretinal space. The magnification and wide field of view provided by a fundus contact lens and the fundus camera are the preferred methods for visualizing these worms but may require prolonged and repeated examinations that are troublesome mainly because of patients' young age and poor fixation. Early diagnosis of the disease is important because destruction of the worm with laser photocoagulation prevents further loss of visual function and occasionally can be followed by improvement in vision.7

We used the scanning laser ophthalmoscope (SLO) to identify live nematodes in patients with DUSN, and we describe several distinct advantages of the SLO system over conventional photography.

We used an SLO (Rodenstock, Ottobrunn-riemerling, Germany) with direct imaging to identify live nematodes in 3 young patients with late-stage DUSN. The blue wavelength was used because at this wavelength, the presence of unbleached photopigment darkens the fundus, so the fovea is darker than the peripheral retina. This produces a high-contrast background for the worm,8 which is white in the picture.

The red wavelength was used to perform red-on-red perimetry simultaneously with infrared imaging so that we could correlate retinal function with the anatomic alterations near the worm.9 The infrared illumination penetrates deeply into the retina and provides information about the retinal and subretinal structures.8 The low power needed to image the retina is virtually invisible to the patient, comfortable, and safe, thereby allowing prolonged examination.

A frame grabber (DT-2861; Data Translation, Inc, Marlboro, Mass) was used to digitize images, display them on the computer monitor in the laser suite, and print them using a digital printer (Kodak XLS 8600; Eastman Kodak Co, Rochester, NY) for clinical documentation. After the purpose, procedures, and consequences of the study were explained to the patients and their guardians, written informed consent was obtained from all.

CASE 1

An 11-year-old girl with the presumed diagnosis of diffuse bilateral subacute neuroretinitis was referred to Bom Jesus Hospital, Ceres, Brazil, for a second opinion. She had previously undergone laser treatment in both eyes without improvement in vision. Her visual acuity levels were 20/200 OD and counting fingers OS. Biomicroscopy revealed a normal anterior segment in both eyes. Signs of mild vitritis associated with a path of RPE degeneration were seen in both eyes; degeneration was worse in the left eye, which also had an extremely pale optic nerve. Multiple crops of evanescent gray-white outer retinal lesions were seen temporal to the macula in the right eye, which had marked RPE involvement. Diffuse bilateral subacute neuroretinitis was suspected. Fundus ophthalmoscopy and careful contact lens biomicroscopy examination did not identify a subretinal worm in either eye because of the poor cooperation and photophobia of the patient. Testing using an SLO revealed a motile subretinal nematode inferotemporal to the fovea in the right eye (Figure 1). No worm was seen in the left eye. We also used perimetry stimulus over the worm to stimulate its movement and define precisely the relation between the fixation point and the worm to plan more accurate laser treatment, considering that the worm was in the macular area (Figure 2).

Place holder to copy figure label and caption
Figure 1.

Argon blue laser (488-nm) scanning laser ophthalmoscopic fundus photograph (direct mode) shows a subretinal, motile, circular nematode inferotemporal to the fovea (arrow) under high magnification(20° field).

Graphic Jump Location
Place holder to copy figure label and caption
Figure 2.

A, Helium-neon laser (633-nm) perimetry scanning laser ophthalmoscopic fundus photograph (direct mode) over the worm shows a poorly defined preferred retinal locus for fixation inferior to the worm (black cross). The black As indicate absolute scotomas, and the white As indicate the stimulus points seen by the patient. B, Infrared laser diode (780-nm) scanning laser ophthalmoscopic picture (direct mode) shows the motile, subretinal, snakelike nematode (arrow) (20° field).

Graphic Jump Location

Argon green laser treatment was applied inferotemporally to the fovea in the right eye where the motile 450- to 600-µm nematode was found, and the retina was mapped by the SLO examination. The results of laboratory investigations were negative. A stool sample was free of ova and parasites. There was no history of cutaneous larval migrans. One month after laser treatment, the patient's visual acuity improved to 20/60 OD; visual acuity in the left eye remained unchanged.

CASE 2

An 8-year-old boy was first seen in January 1999 with a history of vision loss in the right eye resulting from a diagnosis of "retinal lesions" made by his ophthalmologist 1 year previously. His visual acuity levels were 20/400 OD and 20/20 OS. There was no afferent pupillary defect in either eye. Bilateral intraocular pressure was 13 mm Hg. Biomicroscopy showed a normal anterior segment in both eyes and vitreous cells in the right eye. The right fundus examination showed a pale optic nerve, narrowing of the retinal vessels, and focal plus diffuse RPE degeneration. The left fundus was normal. Diffuse unilateral subacute neuroretinitis was suspected in the right eye, but careful contact lens examination did not identify a motile subretinal worm because of poor patient cooperation. However, argon laser treatment was applied to the superior temporal retina in 2 small areas where we suspected that a small worm might be present. After 4 weeks of laser treatment, visual acuity was unchanged(20/400 OD), and no worm was seen. In December 2000, the patient returned. Visual acuity remained 20/400 OD. An SLO examination identified a motile 550- to 650-µm nematode inferonasally in the right eye. The worm's movements were easily seen on the SLO video monitor (Figure 3) and were recorded on videotape. The subretinal worm was destroyed by using laser photocoagulation. The patient was lost to follow-up.

Place holder to copy figure label and caption
Figure 3.

Argon blue laser (488-nm) scanning laser ophthalmoscopic composite fundus photographs (direct mode) of the right eye show the various shapes of the subretinal motile nematode inferonasally(arrows) and demonstrate its coiling and uncoiling movements.

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CASE 3

A 15-year-old girl had an 18-month history of progressive visual loss in the left eye. An ophthalmologist who examined her initially diagnosed optic nerve atrophy. There was no history of ocular inflammation or pain. The patient complained of occasional headaches. Visual acuity levels were 20/20 OD and hand motions OS. There was a relative afferent pupillary defect in the left eye. Intraocular pressure measurements and anterior segment biomicroscopic findings were normal in both eyes. A few cells were seen in the anterior vitreous in the left eye. The left fundus had severe optic nerve atrophy, narrowing of the retinal vessels, and marked RPE degeneration in the posterior pole. The electroretinogram was severely reduced (B wave < A wave). Diffuse unilateral subacute neuroretinitis was suspected in the left eye, and a motile 400- to 500-µm subretinal nematode was found inferotemporally during SLO examination(Figure 4). The nematode was destroyed using continuous argon green laser treatments (150-200 mW, 150-µm spot size). The patient was lost to follow-up.

Place holder to copy figure label and caption
Figure 4.

Helium-neon laser (633-nm) scanning laser ophthalmoscopic fundus photograph (direct mode) of the left eye shows the subretinal motile nematode (arrow) inferotemporally (40° field).

Graphic Jump Location

The SLO uses a novel optical principle to obtain high-quality images of the human retina.10,11 The instrument enables several physicians to view the ocular fundus simultaneously. This is potentially beneficial for finding areas of special interest during examination and for facilitating the training of young physicians in the techniques needed to recognize the worm in patients with late-stage DUSN. The instant feedback that the video provides allows the examiner to optimize laser power and video gain settings and to examine areas of special interest using high magnification.

The contrast of the features in the image can be improved by using the confocal imaging system. We used direct-mode imaging with a circular aperture; the smaller the aperture, the more the image is determined from directly reflected or backscattered light from the plane of focus. Unique to scanning laser tomography, crops of evanescent gray-white outer retinal lesions were seen at different depths, as described with exudative features in RPE detachment.12,13

The SLO video output provides a retinal image that can be reviewed dynamically and repeatedly on video, and thus, a vital frame is unlikely to be missed. This extra temporal information allows clinicians to perceive events not visible in standard static photographs. In clinical examination, the areas of retinal edema obscure the worm and its movements, which are important for identification. Patients with DUSN are frequently children or young adults with an affected retina and photophobia, so it is difficult for them to cooperate during the long examination necessary to locate a small worm. The SLO provides for safe and comfortable examination and thus improves patient cooperation. In clinical examination, a slitlamp is used, which provides only a partial view of the retina. An SLO can display the entire posterior pole live on a video monitor.

The results of an SLO examination are available instantly, allowing immediate laser treatment. This is important in patients with DUSN because continuous movement of the worm across the eye causes further damage to the neuroretina. Immediately after laser treatment, digitized SLO images allow production of simple overlays to confirm that laser treatments completely destroyed the worm. Early diagnosis of the location of the worm is fundamental in the treatment of DUSN and occasionally provides a better visual prognosis, as seen in case 1.

In summary, careful clinical examination by skilled ophthalmologists still plays a key role in the diagnosis of DUSN. The SLO technique, a new method for identifying live nematodes in DUSN, has several distinct advantages over conventional photography and might allow better management of this disease in young patients.

Accepted for publication October 17, 2001.

This study was supported by Fundação de Amparo à Pesquisa, Saõ Paulo (Dr Moraes).

Corresponding author and reprints: Lúcio R. Moraes, MD, Centro Brasileiro de Cirurgia de Olhos, Av. T2 n° 401 Setor Bueno, Goiânia—Goiás 74210-010, Brazil (e-mail: moraesl@terra.com.br).

Gass  JDMGilbert  WR  JrGuerry  RKScelfo  R Diffuse unilateral subacute neuroretinitis. Ophthalmology. 1978;85521- 545
Gass  JDMBraunstein  RA Further observations concerning the diffuse unilateral subacute neuroretinitis syndrome. Arch Ophthalmol. 1983;1011689- 1697
Cunha de Souza  ELustosa da Cunha  SGass  JDM Diffuse unilateral subacute neuroretinitis in South America. Arch Ophthalmol. 1992;1101261- 1263
Cunha de Souza  EAbujamra  SNakashima  YGass  JDM Diffuse bilateral subacute neuroretinitis: first patient with documented nematodes in both eyes. Arch Ophthalmol. 1999;1171349- 1351
Gass  JDM Stereoscopic Atlas of Macular Diseases: Diagnosis and Treatment. 24th St Louis, Mo Mosby–Year Book Inc1997;622- 628
Cialdini  APCunha de Souza  EAvila  MP The first South American case of diffuse unilateral subacute neuroretinitis caused by a large nematode. Arch Ophthalmol. 1999;1171431- 1432
Raymond  LAGutierrez  YStrang  LE  et al.  Living retinal nematode (filarial-like) destroyed with photocoagulation. Ophthalmology. 1978;85944- 949
Elsner  AEBurns  SAWeiter  JJDelori  FC Infrared imaging of subretinal structures in the human ocular fundus. Vision Res. 1996;36191- 205
Chen  JFElsner  AEBurns  SB  et al.  The effect of eye shape on retinal responses. Clin Vis Sci. 1992;7521- 530
Webb  RHHughes  GWDelori  FC Confocal scanning laser ophthalmoscope. Appl Opt. 1987;261492- 1499
Webb  RHHughes  GW Scanning laser ophthalmoscope. IEEE Trans Biomed Eng. 1981;28488- 492
Elsner  AEMoraes  LBeausencourt  E  et al.  Scanning laser reflectometry of retinal and subretinal tissues. Opt Express. 2000;6243- 250
Kunze  CElsner  AEBeausencourt  E  et al.  Spatial extent of pigment epithelial detachments in age-related macular degeneration. Ophthalmology. 1999;1061830- 1840

Figures

Place holder to copy figure label and caption
Figure 1.

Argon blue laser (488-nm) scanning laser ophthalmoscopic fundus photograph (direct mode) shows a subretinal, motile, circular nematode inferotemporal to the fovea (arrow) under high magnification(20° field).

Graphic Jump Location
Place holder to copy figure label and caption
Figure 2.

A, Helium-neon laser (633-nm) perimetry scanning laser ophthalmoscopic fundus photograph (direct mode) over the worm shows a poorly defined preferred retinal locus for fixation inferior to the worm (black cross). The black As indicate absolute scotomas, and the white As indicate the stimulus points seen by the patient. B, Infrared laser diode (780-nm) scanning laser ophthalmoscopic picture (direct mode) shows the motile, subretinal, snakelike nematode (arrow) (20° field).

Graphic Jump Location
Place holder to copy figure label and caption
Figure 3.

Argon blue laser (488-nm) scanning laser ophthalmoscopic composite fundus photographs (direct mode) of the right eye show the various shapes of the subretinal motile nematode inferonasally(arrows) and demonstrate its coiling and uncoiling movements.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 4.

Helium-neon laser (633-nm) scanning laser ophthalmoscopic fundus photograph (direct mode) of the left eye shows the subretinal motile nematode (arrow) inferotemporally (40° field).

Graphic Jump Location

Tables

References

Gass  JDMGilbert  WR  JrGuerry  RKScelfo  R Diffuse unilateral subacute neuroretinitis. Ophthalmology. 1978;85521- 545
Gass  JDMBraunstein  RA Further observations concerning the diffuse unilateral subacute neuroretinitis syndrome. Arch Ophthalmol. 1983;1011689- 1697
Cunha de Souza  ELustosa da Cunha  SGass  JDM Diffuse unilateral subacute neuroretinitis in South America. Arch Ophthalmol. 1992;1101261- 1263
Cunha de Souza  EAbujamra  SNakashima  YGass  JDM Diffuse bilateral subacute neuroretinitis: first patient with documented nematodes in both eyes. Arch Ophthalmol. 1999;1171349- 1351
Gass  JDM Stereoscopic Atlas of Macular Diseases: Diagnosis and Treatment. 24th St Louis, Mo Mosby–Year Book Inc1997;622- 628
Cialdini  APCunha de Souza  EAvila  MP The first South American case of diffuse unilateral subacute neuroretinitis caused by a large nematode. Arch Ophthalmol. 1999;1171431- 1432
Raymond  LAGutierrez  YStrang  LE  et al.  Living retinal nematode (filarial-like) destroyed with photocoagulation. Ophthalmology. 1978;85944- 949
Elsner  AEBurns  SAWeiter  JJDelori  FC Infrared imaging of subretinal structures in the human ocular fundus. Vision Res. 1996;36191- 205
Chen  JFElsner  AEBurns  SB  et al.  The effect of eye shape on retinal responses. Clin Vis Sci. 1992;7521- 530
Webb  RHHughes  GWDelori  FC Confocal scanning laser ophthalmoscope. Appl Opt. 1987;261492- 1499
Webb  RHHughes  GW Scanning laser ophthalmoscope. IEEE Trans Biomed Eng. 1981;28488- 492
Elsner  AEMoraes  LBeausencourt  E  et al.  Scanning laser reflectometry of retinal and subretinal tissues. Opt Express. 2000;6243- 250
Kunze  CElsner  AEBeausencourt  E  et al.  Spatial extent of pigment epithelial detachments in age-related macular degeneration. Ophthalmology. 1999;1061830- 1840

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