Open Access

Three-dimensional spectral domain optical coherence tomography and light microscopy of an intravitreal parasite

  • Aziz A. Khanifar1,
  • Michael J. Espiritu1,
  • Jane S. Myung1,
  • Grant D. Aaker1,
  • Audrey N. Schuetz2,
  • Donald J. D’Amico1 and
  • R. V. Paul Chan1, 3Email author
Journal of Ophthalmic Inflammation and Infection20155:33

https://doi.org/10.1186/s12348-015-0064-x

Received: 27 August 2015

Accepted: 5 November 2015

Published: 19 November 2015

Abstract

Background

Various imaging modalities play a role in diagnosing parasitic infections of the eye. We describe the spectral domain optical coherence tomography (SD-OCT) findings of an intravitreal parasite with subsequent evaluation by light microscopy.

Findings

This is a case report of a 37-year-old Ecuadorian man who presented with uveitic glaucoma and a new floater in his left eye for 1 week’s duration. Full ophthalmic examination revealed an intravitreal parasite. Color fundus photography, fluorescein angiography (FA), ocular ultrasonography (US), and SD-OCT were performed. The parasite was removed via 23-gauge pars plana vitrectomy and sent to pathology for evaluation.

Color fundus photography and ocular ultrasonography demonstrated an elongated foreign body within the vitreous above the retina. FA demonstrated minimal vascular changes in the vicinity of the parasite. SD-OCT was utilized to visualize the parasite and to create a three-dimensional (3D) image. The parasite was determined to be most consistent with Gnathostoma spp. by morphologic analysis.

Conclusions

This is the first reported case of SD-OCT of an intravitreal parasite with corresponding evaluation by pathology. SD-OCT allows non-invasive, high-resolution visualization and 3D reconstruction of parasitic anatomy which may help establish tomographic criteria for species identification.

Keywords

Gnathostomiasis Gnathostoma Ophthalmomyiasis Optical coherence tomography Parasitic infection Retinal imaging

Findings

Introduction

Intraocular parasites are uncommon occurrences in the USA. Diagnosis is dependent on reliable history of ingested foods, geographic location, season, and direct visualization of the parasite with ophthalmoscopy. Various imaging modalities have also been applied in the study of intraocular parasites such as fluorescein angiography. Ultrasound biomicroscopy has been used to localize larvae when not seen on dilated fundus examination [1], and scanning electron microscopy has aided morphological study for species determination [2, 3].

While optical coherence tomography (OCT) has been utilized in visualizing tracks of nonspecific cutaneous larva migrans through the epidermis [4], its capabilities have yet to be explored with regard to complete visualization of an intraocular helminthic infection. We report a case in which spectral domain optical coherence tomography (SD-OCT) imaging of an intravitreal parasite was performed. The clinical presentation and pathological findings are most consistent with Gnathostoma spp.

Case report

A 37-year-old Ecuadorian immigrant presented to the New York-Presbyterian Hospital Emergency Department with a 3-day history of redness, pain, and hazy vision in his left eye. He denied flashes, photophobia, or discharge in either eye. He had no complaints in his right eye.

Two weeks prior to presentation, he experienced fevers, nasal congestion, and muscle aches, which spontaneously resolved. He also admitted to recently seeing a curved floater in his left eye. His past medical history was significant only for Bell’s palsy on the left in 2004, which had resolved spontaneously without ocular complications. His last tuberculin skin test was 3 years prior to presentation and was negative. He denied any risk factors for HIV. His past social history revealed that he immigrated to the USA from Ecuador 13 years ago and has not been back to Ecuador for 9 years. He denied any other travel, farm work, or extended contact with animals. The patient worked in a local restaurant as a cook, handling raw beef, pork, poultry, and both saltwater and freshwater fish with his bare hands. He reported that his duties include preparing the tuna tartar, and he usually eats any leftover food.

On examination, his visual acuity was 20/20 in both eyes with pinhole. Intraocular pressure (IOP) was 12 and 35 mm Hg in his right and left eyes, respectively. Pupils, motility, confrontational visual fields, and external exam were within normal limits bilaterally. Slit lamp biomicroscopy and dilated fundus examination were normal for the right eye. In the left eye, the conjunctiva and sclera were quiet, and the cornea had microcystic edema and fine keratic precipitates. Cells were present in the anterior chamber, but there was no hypopyon. The iris and lens were normal. Dilated fundus exam revealed a peripheral operculated hole in the left eye and a single linear object measuring approximately 3 mm in length floating in the nasal vitreous. The object appeared to have a white disc followed by a whitening of the body on one end and a white pointed tip preceded by a reddish brown coloration of the body at the other end (Fig. 1). No vitritis, papillitis, vasculitis, retinitis, and other retinal breaks or detachments were noted. Ultra-widefield fluorescein angiography demonstrated mild vascular sheathing in the region where the parasite was originally seen (Fig. 2). Ocular ultrasonography verified that the object was not in contact with the retinal surface (Fig. 3). Using the Topcon 3D OCT-1000 (Topcon Medical Systems, Paramus, NJ), the intravitreal object was imaged (Fig. 4a, b and Additional file 1: Video 1). Three-dimensional (3D) reconstructions using the OCT B-scans were also created (Fig. 5a, b and Additional file 2: Video 2). Review of the scans demonstrated a tubular structure with a central lumen overlying the nasal retina. Superiorly, the lumen contained hyper-reflective material (Fig. 4a), whereas the inferior lumen was hypo-reflective (Fig. 4b).
Fig. 1

a Wide-angle color fundus photograph of the patient’s left eye demonstrating the parasite (white oval) within the vitreous and nasal to the optic disc. b Higher magnification color photograph of the intravitreal parasite

Fig. 2

Wide-angle fluorescein angiogram demonstrating vascular sheathing (white arrow) in the region where the parasite was initially visualized

Fig. 3

Ocular ultrasonography demonstrating the parasite (white arrow) within the vitreous. Note that the parasite is not in contact with the retina

Fig. 4

Spectral domain optical coherence tomography (SD-OCT) images of the parasite demonstrating two concentric circles within the vitreous above the retina. Note that the inner circle is hyper-reflective superiorly (top image) and hypo-reflective inferiorly (bottom image)

Fig. 5

a Three-dimensional reconstruction of spectral domain optical coherence tomography (SD-OCT) images of the intravitreal parasite. b Additional view of SD-OCT image from different angles

Further diagnostic evaluation of the patient revealed peripheral eosinophilia, and magnetic resonance imaging of the brain was negative for cerebral larvae. Based on its appearance, gnathostomiasis was high on the differential diagnosis. A 23-gauge pars plana vitrectomy with removal of the foreign body was performed. Intraoperatively, the presumed worm was noted to be associated with superficial retinal hemorrhages and resist aspiration. The worm was eventually aspirated with a vitreous cutter using aspiration only. The specimen, within the tip of the vitreous cutter, was sent for microscopic evaluation by the Department of Pathology and Laboratory Medicine at New York-Presbyterian Hospital. The patient was discharged on oral ivermectin and recovered well.

Macroscopically, the single larva was light red-brown in color and 3 mm in length when viewed under a dissecting microscope (Fig. 6). Only a portion of the worm was available for examination after removal from the vitreous cutter, with a portion of the cuticle removed. Through examination of the remaining worm, including the probable gastrointestinal tract and the remnant of the anterior portion of the worm, a differential diagnosis was generated. Based on the size of the larva and the minute spines present on the cuticular armature of the head bulb on the anterior portion of the worm (Fig. 7), Gnathostoma spp. was the most likely diagnosis. The differential included bot fly larva or Thelazia spp. based on ocular localization, but the organism shape and size were not consistent with those organisms.
Fig. 6

Light microscopy photograph of the parasite removed from the patient’s vitreous cavity. The cuticle has been partially removed

Fig. 7

Higher magnification photograph of the rostral portion of the parasite demonstrating minute cuticular spines encircling the cuticular armature of the head bulb

Discussion

To our knowledge, this is the first reported case of intravitreal 3D SD-OCT imaging of a parasite in vivo and subsequent evaluation with light microscopy. Other investigators have utilized OCT to follow complications of parasitic infestation, but imaging of the actual parasite has rarely been reported [511].

Gnathostomiasis is a rare parasitic infection that can affect multiple organ systems, including the eye. This zoonosis results from accidental ingestion of immature Gnathostoma larvae, a type of roundworm endemic to Southeast Asia and Latin America. The most common clinical presentation is dermatological—a cutaneous larva migrans [2]. However, intraocular gnathostomiasis is uncommon and can be localized to the anterior segment, retina, and vitreous cavity [1219].

Myiasis is another parasitic infection that can affect the skin and the eye (ophthalmomyiasis). The causative organism is the immature larva of any fly of the order Diptera. Invasion of the globe is classified as ophthalmomyiasis interna anterior/posterior [20]. The clinical presentation of ophthalmomyiasis interna posterior (OIP) is very similar to that of intraocular gnathostomiasis, including uveitis (with or without eosinophilia) and self-limiting periorbital swelling [21]. For cases of OIP in which the larva is located within the subretinal space, photocoagulation may be used with minimal or no resultant inflammation [22, 23]. The subretinal pigmented tracks formed from larval migration within the subretinal space are pathognomonic for OIP [24].

Regarding the intraocular parasite of this patient, the SD-OCT findings are consistent with the findings on ophthalmoscopy. The internal reflectivity of the superior segments varies compared to that of the inferior segments. The hyper-reflectivity superiorly likely corresponds to a hyper-cellular esophagus represented as whitening grossly, and the hypo-reflectivity inferiorly corresponds to a relatively hypo-cellular intestinal tract represented as reddish brown coloration grossly. Closer observation of the inferior scans of the parasite reveals hyper-reflective lines connecting the outer lumen with the inner lumen. These hyper-reflective lines may represent lateral chords, and this configuration may be more suggestive of gnathostomiasis [25].

The high-resolution imaging of the worm and the acquisition of multiple images aligned along the body of the worm would be extremely difficult if not impossible with time-domain OCT.

SD-OCT with its high-speed scanning not only allows visualization of microscopic detail in vivo, but also allows volumetric, three-dimensional imaging. The Topcon 3D OCT-1000 (Topcon Medical Systems, Paramus, NJ) was able to render a three-dimensional representation of the worm in the vitreous. While patient history and visualization of the worm are helpful in diagnosing intraocular parasites, microscopic diagnosis is more definitive. SD-OCT may play an adjunctive role in identifying intraocular parasitic species prior to surgical removal and should be considered as part of the diagnostic imaging evaluation.

Abbreviations

3D: 

three-dimensional

OIP: 

ophthalmomyiasis interna posterior

SD-OCT: 

spectral domain optical coherence tomography

Declarations

Acknowledgements

Support was provided by the St. Giles Foundation (RVPC), Departmental Grant from Research to Prevent Blindness (RVPC, AAK, JSM, GDA, MJE, DJD).

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors’ Affiliations

(1)
Department of Ophthalmology, Weill Cornell Medical College
(2)
Department of Pathology and Laboratory Medicine, Weill Cornell Medical College
(3)
Department of Ophthalmology and Visual Sciences, Illinois Eye and Ear Infirmary, University of Illinois at Chicago

References

  1. Bhende M, Biswas J, Gopal L (2005) Ultrasound biomicroscopy in the diagnosis and management of intraocular gnathostomiasis. Am J Ophthalmol 140:140–142View ArticlePubMedGoogle Scholar
  2. Rusnak JM, Lucey DR (1993) Clinical gnathostomiasis: case report and review of the English-language literature. Clin Infect Dis 16:33–50View ArticlePubMedGoogle Scholar
  3. Funata M, Custis P, de la Cruz Z, de Juan E, Green WR (1993) Intraocular gnathostomiasis. Retina 13:240–244View ArticlePubMedGoogle Scholar
  4. Morsy H, Mogensen M, Thomsen J, Thrane L, Andersen PE, Jemec GB (2007) Imaging of cutaneous larva migrans by optical coherence tomography. Travel Med Infect Dis 5:243–247View ArticlePubMedGoogle Scholar
  5. Gomes AH, Garcia CA, Segundo Pde S, Garcia Filho CA, Garcia AC (2009) Optic coherence tomography in a patient with diffuse unilateral subacute neuroretinitis. Arq Bras Oftalmol 72:185–188View ArticlePubMedGoogle Scholar
  6. do Lago A, Andrade R, Muccioli C, Belfort R Jr (2006) Optical coherence tomography in presumed subretinal Toxocara granuloma: case report. Arq Bras Oftalmol 69:403–405View ArticlePubMedGoogle Scholar
  7. Suzuki T, Joko T, Akao N, Ohashi Y (2005) Following the migration of a Toxocara larva in the retina by optical coherence tomography and fluorescein angiography. Jpn J Ophthalmol 49:159–161View ArticlePubMedGoogle Scholar
  8. Higashide T, Akao N, Shirao E, Shirao Y (2003) Optical coherence tomographic and angiographic findings of a case with subretinal Toxocara granuloma. Am J Ophthalmol 136:188–190View ArticlePubMedGoogle Scholar
  9. Khatibi A, Amini P, Goldbaum MH (2013) Parasite in a young girl from Vietnam presenting as a golden foveal lesion: submacular fly larva or nematode? Retin Cases Brief Rep 7(1):32–4View ArticlePubMedGoogle Scholar
  10. Ahmed E, Houston MA, Husain D (2010) High-definition spectral domain OCT of a subretinal nematode. Eye (Lond) 24(2):393–4View ArticleGoogle Scholar
  11. Masudi A, Soheilian M, Nourinia R, Soheilian R, Peyman GA (2013) Spectral-domain optical coherence tomography appearance of a retinal nematode. Ophthalmic Surg Lasers Imaging Retina Online 44:E17–9Google Scholar
  12. Bathrick ME, Mango CA, Mueller JF (1981) Intraocular gnathostomiasis. Ophthalmology 88:1293–1295View ArticlePubMedGoogle Scholar
  13. Biswas J, Gopal L, Sharma T, Badrinath SS (1994) Intraocular Gnathostoma spinigerum: clinicopathologic study of two cases with review of literature. Retina 14:438–444View ArticlePubMedGoogle Scholar
  14. Sasana K, Ando F, Nagasaka T, Kidokoro T, Kawamoto F (1994) A case of uveitis due to Gnathostoma migration into the vitreous cavity. Nippon Ganka Gakkai Zasshi 98:1136–1140Google Scholar
  15. Basak SK, Sinha TK, Bhattacharya D, Hazra TK, Parikh S (2004) Intravitreal live Gnathostoma spinigerum. Indian J Ophthalmol 52:57–58PubMedGoogle Scholar
  16. Bhattacharjee H, Das D, Medhi J (2007) Intravitreal gnathostomiasis and review of literature. Retina 27:67–73View ArticlePubMedGoogle Scholar
  17. Sujata DN, Renu BS (2013) Intraocular gnathostomiasis from coastal part of Maharashtra. Trop Parasitol 3(1):82–4PubMed CentralView ArticlePubMedGoogle Scholar
  18. Pillai GS, Kumar A, Radhakrishnan N, Maniyelil J, Shafi T, Dinesh KR, Karim S (2012) Intraocular gnathostomiasis: report of a case and review of literature. Am J Trop Med Hyg 86(4):620–3PubMed CentralView ArticlePubMedGoogle Scholar
  19. Yang JH, Kim M, Kim ES, Na BK, Yu SY, Kwak HW (2012) Imported intraocular gnathostomiasis with subretinal tracks confirmed by western blot assay. Korean J Parasitol 50(1):73–8PubMed CentralView ArticlePubMedGoogle Scholar
  20. Behr C (1920) Ophthalmomyiasis interna and externa. Klin Mbl Augenh 64:161–180Google Scholar
  21. Kearney MS, Nilssen AC, Lyslo A, Syrdalen P, Dannevig L (1991) Ophthalmomyiasis caused by the reindeer warble fly larva. J Clin Pathol 44:276–284PubMed CentralView ArticlePubMedGoogle Scholar
  22. Fitzgerald CR, Rubin ML (1974) Intraocular parasite destroyed by photocoagulation. Arch Ophthalmol 91:162–164View ArticlePubMedGoogle Scholar
  23. Forman AR, Cruess AF, Benson WE (1984) Ophthalmomyiasis treated by argon-laser photocoagulation. Retina 4:163–165View ArticlePubMedGoogle Scholar
  24. Gass JDM, Lewis RA (1976) Subretinal tracts in ophthalmomyiasis. Arch Ophthalmol 94:1500–1505View ArticlePubMedGoogle Scholar
  25. Centers for Disease Control and Prevention (n.d.). Gnathostomiasis. Retrieved from http://www.dpd.cdc.gov/dpdx/HTML/ImageLibrary/GL/Gnathostomiasis/body_Gnathostomiasis_il4.htm. Accessed on August 7, 2015.

Copyright

© Khanifar et al. 2015