1040-5488/14/9111-e267/0 VOL. 91, NO. 11, PP. e267Ye273 OPTOMETRY AND VISION SCIENCE Copyright * 2014 American Academy of Optometry
CLINICAL CASE
Toxocara Optic Neuropathy after Ingestion of Raw Meat Products Hee Kyung Yang*, Se Joon Woo*, and Jeong-Min Hwang*
ABSTRACT Purpose. To report Toxocara optic neuropathy in five men with histories of ingestion of raw meat, liver, or blood. Case Report. Five men in their 30s to 60s presented with unilateral visual disturbance. All five had a history of ingesting raw meat, liver, or blood products. All five men presented with optic disc edema and three also showed granulomatous infiltration of the retina. With Goldmann or Humphrey visual field testing, two patients showed central scotomas and two exhibited arcuate defects. Serum eosinophil count and total IgE were elevated in four patients. Serum enzyme-linked immunosorbent assay testing was positive for Toxocara canis IgG in all five cases. Conclusions. This report shows the variable clinical presentations of Toxocara optic neuropathy and the importance of questioning for a history of eating raw meat and blood products as a risk factor. (Optom Vis Sci 2014;91:e267Ye273) Key Words: Toxocara optic neuropathy, raw meat, ocular toxocariasis, toxocariasis, neuroretinitis
T
oxocariasis is a nematode infection by Toxocara canis or Toxocara cati.1Y22 Domesticated cats and dogs are the usual primary host and humans are infected mainly through the ingestion of Toxocara eggs in soil contaminated by dog and cat feces.1,2 Children are at risk of infection by eating dirt or frequent contact with puppies; thus, it has been reported that toxocariasis mainly affects children.1,2 On the other hand, raw meat products are also easily contaminated with embryonated helminthic eggs. There are many situations for adults to consume raw meat as a variety of cultural foods, such as Parisa (South Texas), Carne Apache (Mexico), Crudos (Chile), Mett (Germany), Steak tartare (France), Basashi (Japan), Ossenworst (The Netherlands), Beef Carpaccio (Italy), Asbeh nayeh (Lebanon), Yookhwe (Korea), Koi Soi (Thailand), or Bo Tai Chanh (Vietnam), which may also be the route for Toxocara infection. The most common ophthalmic sign of ocular toxocariasis is subretinal granulomas involving the macula and peripheral retina.1Y12 Although there are a few case reports of toxocariasis involving the optic nerve in the literature,3Y7 there has not been a published case series. The purpose of this case series was to report different histories and clinical manifestations of
*MD Department of Ophthalmology, Seoul National University College of Medicine, Seoul National University Bundang Hospital, Seongnam, Korea (all authors).
toxocara optic neuropathy. All cases showed unilateral optic nerve involvement.
CASE REPORTS Case 1 A 31-year-old man presented with sudden visual blurring and pain on eye movement in the right eye (OD) (Table 1). He had a pet dog and frequently ate raw minced beef and raw cow liver. His visual acuity was 20/200 OD. Fundus examination showed edema and whitish infiltration of the optic disc with subtle vitritis OD (Fig. 1). Optical coherence tomography showed a white intraretinal lesion near the disc protruding from the retinal surface into the vitreous (Fig. 2). Goldmann perimetry showed a large central scotoma. Hardy, Rand, and Rittler (HRR) color vision testing showed a strong blue-yellow defect. Systemic underlying causes of unilateral disc edema including autoimmune diseases, inflammatory conditions, cancer masquerade syndromes, and infectious etiologies were considered. The results of an extensive serology and microbiological screening, including complete blood count; erythrocyte sedimentation rate; C-reactive protein; antiYdouble-stranded DNA antibodies; rheumatoid factor; complement components; anticardiolipin antibodies; angiotensin-converting enzyme; antineutrophil cytoplasmic antibodies; and immunoglobulins (Ig) G, A, and M; were unremarkable. Microbiological tests were negative
Optometry and Vision Science, Vol. 91, No. 11, November 2014
Copyright © American Academy of Optometry. Unauthorized reproduction of this article is prohibited.
e268 Toxocara Optic Neuropathy after Ingestion of Raw MeatVYang et al. TABLE 1.
Demographics and clinical findings of five patients Patient no. 1
2
3
4
5
Male 36 R Raw cow liver, minced beef j Sudden visual loss
Male 68 R Raw cow stomach, liver, minced beef j Sudden visual loss
Male 45 L Raw cow liver, deer blood j Sudden visual loss
Ocular pain Initial VA Final VA Visual field
Male 31 R Raw cow liver, minced beef Dog Progressive visual loss + 20/200 FC Central scotoma
j 20/800 20/50 Central scotoma
j 20/800 20/40 Not done
Color vision Granuloma Disc edema Additional features
Strong BY defect + ++ Circumpapillary choroidal folds
Achromatopsia + + Macular edema and exudate
Not done + + Macular edema and exudate
+ 20/100 20/30 Inferior arcuate scotoma Normal j + Macular edema and exudate
0.512 5.8
0.444 6.8
0.463 5.6
1.676 6.8
Male 49 R Raw liver of cow and rabbit Y Inferotemporal visual field defect + 20/20 20/100 Superior and inferior arcuate scotoma Normal + ++ Circumpapillary choroidal folds, macular edema/exudate 1.380 3.2
415.3 Oral prednisolone, vitrectomy, later albendazole
338.6 Oral prednisolone, vitrectomy, later albendazole
104.3 Oral prednisolone, later albendazole
20.03 Oral prednisolone, later albendazole
+ 16
+ 31
862.1 Oral prednisolone, early albendazole, intravitreal bevacizumab j 26
+ 4
+ 9
Epiretinal membrane, temporal pallor
Epiretinal membrane, temporal pallor
Mild temporal pallor, no granuloma
Temporal pallor, dot hard exudates
Temporal pallor, dot hard exudates
Sex Age, y Affected eyes History of raw food Pet Symptom
T. canis IgG titer* Eosinophil counts, %† Total IgE, IU/mL‡ Treatment
Recurrence Duration of follow-up, mo Final fundus findings
*Normal range, 0 to 0.250 optical densities.13 †Normal range, 1 to 5%. ‡Normal range, 0 to 100 IU/mL. VA, visual acuity; FC, finger count; BY, blue yellow.
for syphilis, Lyme disease, interferon-F release assay, toxoplasmosis, bartonella, herpes simplex virus, varizella zoster virus, and HIV. After high-dose steroid therapy, visual acuity recovered to 20/20 OD and optic disc edema resolved, leaving a granulomatous infiltration on the optic disc and lipid exudates within the macula. However, after steroid tapering, vision decreased to counting fingers and new severe vitritis with retinal granulomatous lesions involving the macula were seen (Fig. 1). He underwent pars plana vitrectomy; however, ocular inflammation waxed and waned with the use of systemic steroids. At that time, we performed additional microbiological testing and serum enzyme-linked immunosorbent assay (ELISA) titers were positive for T. canis IgG. Serum eosinophil count was slightly elevated, and total IgE levels were increased. Administration of oral albendazole 400 mg bid for 2 weeks was followed with a tapered dose of continuous steroid therapy (initial dose of 0.5 mg/kg
per day). After treatment, the inflammation was well controlled without significant recurrence. However, because of scar tissue formation involving the fovea, his visual acuity remained counting fingers.
Case 2 A 36-year-old man presented with sudden visual loss that developed 4 days prior without ocular pain OD. He did not have a pet and used to eat raw cow liver and minced beef. His visual acuity was 20/800 OD. Fundus examination revealed disc edema and whitish infiltration of the optic disc with retinal hemorrhage and exudates involving the macula (Fig. 1). Optical coherence tomography showed a white intraretinal granulomatous lesion (Fig. 2). Goldmann perimetry showed a large central and inferior scotoma. He did not pass any of the color plates of the HRR test and could only recognize the screening plate
Optometry and Vision Science, Vol. 91, No. 11, November 2014
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Toxocara Optic Neuropathy after Ingestion of Raw MeatVYang et al.
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FIGURE 1. Fundus photographs at initial presentation before treatment and 1 to 2 months later. Cases 1 to 3 showed optic disc edema and granulomas of the peripapillary retina. Cases 4 and 5 showed optic disc edema without granuloma at initial presentation, but vitritis and macular exudates eventually developed. Granulomas newly appeared in case 5. Optometry and Vision Science, Vol. 91, No. 11, November 2014
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e270 Toxocara Optic Neuropathy after Ingestion of Raw MeatVYang et al.
FIGURE 2. Optical coherence tomography. Cases 1 to 3 showed optic disc edema with whitish granulomatous lesions (arrows) on the disc or peripapillary retina. Cases 4 and 5 showed optic disc edema without any demonstrable lesion of granuloma at initial presentation. However, granulomas newly developed in case 5 (arrow).
of the Ishihara color vision test. Ocular inflammation subsided with the use of oral prednisolone. Two months later, vitritis, macular exudates, and new granulomatous lesions in the macula developed. He underwent pars plana vitrectomy and the ocular inflammation waxed and waned with the use of systemic steroids. An extensive laboratory screening panel showed negative results except for positive serum ELISA titers for T. canis IgG and elevated serum eosinophil counts and total IgE levels. Administration of oral albendazole 400 mg bid for 2 weeks was followed with a tapered dose of continuous steroid therapy. His visual acuity was limited to 20/50 because of scar tissue formation and photoreceptor disruption in the macula.
Case 3 A 68-year-old man presented with sudden visual loss that developed 1 week prior without ocular pain OD. He did not have a pet and used to eat raw cow stomach, liver, and minced beef. His visual acuity was 20/800 OD. Visual field and color vision testing were not performed. Fundus examination revealed disc edema with peripapillary whitish infiltration and subretinal fluid accumulation that involved the macula OD (Fig. 1). Optical coherence tomography showed a peripapillary intraretinal granulomatous lesion (Fig. 2). Serum ELISA titers were positive for T. canis IgG. Serum eosinophil count and total IgE levels were increased. A month after treatment with albendazole 400 mg bid for 2 weeks
Optometry and Vision Science, Vol. 91, No. 11, November 2014
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Toxocara Optic Neuropathy after Ingestion of Raw MeatVYang et al.
and oral prednisolone, optic disc and macular edema decreased, leaving exudates within the macula. The patient was followed for 26 months without recurrence. Visual acuity remained 20/25 (Fig. 1).
Case 4 A 45-year-old man presented with visual blurring that developed 2 weeks prior preceded by ocular pain in the left eye (OS). He used to eat raw cow liver and deer blood. His visual acuity was 20/100 OS. Fundus examination revealed optic disc edema and hemorrhage without granulomas within the retina OS (Fig. 1). Optical coherence tomography showed no demonstrable granulomatous lesions of the optic disc or macula OS (Fig. 2). Humphrey visual fields showed an inferior arcuate scotoma OS. Results of HRR color vision testing were normal. An initial diagnosis of nonarteritic anterior ischemic optic neuropathy was made and systemic steroids were applied for 5 days. One month later, his visual acuity had decreased to 20/100 and star-shaped retinal exudation in the macula had developed OS. An extensive laboratory screening panel showed negative results except for positive serum ELISA titers for T. canis IgG and increased serum eosinophil counts and total IgE levels. Administration of oral albendazole 400 mg bid for 2 weeks was followed with a tapered dose of continuous steroid therapy. After treatment, the inflammation gradually subsided and visual acuity improved to 20/30.
Case 5 A 49-year-old man presented with inferotemporal visual field defects for 3 to 4 days OD. He ate raw cow and rabbit liver about 6 months prior. Visual acuity was 20/20 and fundus examination showed disc edema, circumpapillary choroidal folds, and dilated tortuous retinal veins OD (Fig. 1). Optical coherence tomography showed no demonstrable granulomatous lesions of the optic nerve or retina. Humphrey visual fields showed arcuate scotomas inferiorly greater than superiorly. The results of the HRR color vision testing were normal. An initial diagnosis of nonarteritic anterior ischemic optic neuropathy was made and systemic steroids were applied for 5 days. Two weeks later, his vision deteriorated to hand motion in the right eye as an optic disc granuloma with macular-star pattern exudates developed (Fig. 1). Optical coherence tomography showed whitish intraretinal lesions near the optic disc and macular subretinal fluid (Fig. 2). An extensive laboratory screening panel was nondiagnostic except for positive serum ELISA titers for T. canis IgG and increased total IgE levels. Serum eosinophil counts were normal. Administration of oral albendazole 400 mg bid for 2 weeks was followed with a tapered dose of steroid therapy. After the treatment, the inflammation subsided without recurrence during 10 months of follow-up. His vision improved to 20/100 with a remnant cecocentral scotoma on perimetry.
DISCUSSION This report represents the largest series of patients with toxocara affecting the optic nerve. The patients were all men in their 30s to 60s who had a history of eating raw meat, liver, or animal blood.
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Domesticated cats and dogs are the usual primary host, but only case 1 had a pet dog. Three of five patients had sudden visual loss. Three of five patients had ocular pain. Four out of five patients presented with loss of their central vision, ranging from 20/100 to 20/800. The fifth patient presented with peripheral visual field loss. Fundus findings included subtle to severe optic disc swelling in all patients, retinal granulomas at initial presentation in three patients, and two delayed onset retinal granulomas after a few weeks. There were circumpapillary choroidal folds in two patients, and eventually all five patients manifested macular exudates. Color vision varied from normal to total achromatopsia. Visual field testing showed central scotomas in two patients and arcuate scotomas in two other patients. Serum ELISA titers were positive for T. canis IgG in all patients. Four of five patients showed elevated eosinophil counts and total IgE antibodies. At presentation, case 2 showed disc edema accompanied by star-patterned macular exudates as did cases 4 and 5 later in their courses. Besides toxocara, this clinical picture can be seen with increased intracranial pressure and ischemic optic neuropathies. Malignant hypertensive retinopathy and central retinal vein occlusion can also result in disc edema with associated macular exudates as can neuroretinitis caused by inflammatory or infectious etiologies. In the presented case series, this list of differentials could be narrowed down based on the clinical presentation and with the appropriate laboratory investigations. Malignant hypertensive retinopathy and increased intracranial pressure usually result in bilateral disc swelling and may be accompanied by symptoms of headache, transient visual obscuration, or pulsatile tinnitus. Hypertensive retinopathy and central retinal vein occlusion usually also manifest with more widespread intraretinal hemorrhages as well as retinal vessel caliber or crossing changes. None of these findings were seen in these cases and none of the patients had increased blood pressure at the time of examination. The infectious and inflammatory causes of neuroretinitis should also be ruled out as part of the laboratory work-up for disc swelling associated with macular exudation. Causative viral agents include mumps, Epstein-Barr virus, HIV, herpes simplex virus, and hepatitis B and C viruses. Although cultures from the vitreous humor, aqueous humor, or cerebral spinal fluid are possible, positive cultures are rare. Other nonviral infectious causes include Bartonella henselae (cat scratch disease), Toxoplasma gondii (toxoplasmosis), Treponema pallidum (syphilis), Leptospira spp. (leptospirosis), Borrelia burgdorferi (Lyme disease), Mycobacterium tuberculosis (tuberculosis), Rickettsia typhi (murine typhus), Brucella spp. (brucellosis), and Histoplasma capsulatum (histoplasmosis). Clinical history is also important when neuroretinitis is suspected. The diagnosis of Lyme disease may be aided by a history of tick bite, cutaneous rash, or migrating musculoskeletal pain. Questions regarding contact with cats should be pursued for cat scratch disease and a thorough sexual history should be taken for risk of syphilitic infection. Rarely, ocular toxocariasis can be definitively diagnosed by direct observation of the larva in the eye. More often, it is diagnosed with a combination of positive serology and clinically observed granulomas of the retina or optic nerve. Detection of serum antitoxocara IgG with an indirect ELISA on the Toxocara larva antigen is diagnostic. Elevated eosinophil counts could also be helpful for the diagnosis of helminthic infection if present.
Optometry and Vision Science, Vol. 91, No. 11, November 2014
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e272 Toxocara Optic Neuropathy after Ingestion of Raw MeatVYang et al.
However, eosinophil counts could be normal or only mildly elevated with ocular toxocariasis. Cases 4 and 5 were unique in that they showed only disc swelling without granulomas at their initial presentation. Their initial visual acuities of 20/100 and 20/20, respectively, were also better than the other cases. Color vision was normal with only arcuate scotomas seen on visual field testing. This mild presentation may represent the early stage of toxocara optic neuropathy and mimics more common optic neuropathies such as anterior ischemic optic neuropathy. Hayashi et al.18 showed that the optic nerve could be a migratory route of T. canis from the brain to the eye in an animal model of Mongolian gerbils. Therefore, cases 4 and 5 may represent the clinical presentation as the T. canis is migrating within the nerve before development of the classic granulomatous response. Therefore, careful follow-up examination over time is mandatory in suspected patients. Based on the observations from this case series, a history of ingesting raw meat or blood products should also raise the suspicion of ocular toxocariasis. Because ocular toxocariasis is relatively rare, suspicion of it as a diagnosis usually requires a typical clinical presentation. Thus, in the absence of visible granuloma, it is difficult to suspect toxocara as the etiology of the optic neuropathy and the diagnosis is dependent on positive serologic tests. Based on the reported cases, toxocara optic neuropathy may be differentiated from other acute optic neuropathies in the following ways: (1) presence of granulomas of the optic nerve or retina, (2) peripapillary subretinal exudation and localized serous retinal detachment, (3) positive serum toxocara IgG assay, (4) history of ingestion of raw meat, and (5) recurrence with vitritis. The preferred management of ocular toxocariasis has not been settled. Corticosteroid is the mainstay for treatment, reducing the inflammatory response and preventing the development of tractional retinal detachment.14,15 Oral prednisolone 1 mg/kg daily for 1 month or more is commonly prescribed. The need for antihelminthics is controversial because of the concern that dead larvae can cause more severe reaction and permanently damage the eye.16 However, Ahn et al.12 found that combined treatment of albendazole (400 mg twice a day for 2 weeks) and oral prednisolone (0.5 to 1 mg/kg per day) significantly lowered the 6-month recurrence rate compared with corticosteroid monotherapy. Albendazole is the drug of choice because it crosses the blood-brain and blood-retina barriers.17 In addition to toxocariasis, raw meat ingestion could result in other intraocular parasitic infections such as gnathostomiasis, toxoplasmosis, cysticercosis, onchocerciasis, and ophthalmomyiasis.19,20 Therefore, patients with any suspicious lesions should be asked about raw meat ingestion. Based on the patient histories taken from the presented case series, no definitive conclusions could be drawn regarding timing of ingestion of the raw meat or blood products and when the eye became involved. Because ingestion of such food likely was a regular part of their diets, only one of the reported patients (case 4) could remember that he had ingested raw cow liver and deer blood specifically 6 months prior. A previous report also demonstrated a patient who developed intraocular gnathostomiasis after ingestion of raw wild boar meat and lobster 8 months prior.23 Toxocara larvae can survive in human tissues over 10 years; therefore, any ingestion up to 10 years can cause ocular toxocariasis.20
There are several important messages from this case series. Although toxocariasis is typically considered a childhood disease, it can affect any age group that ingests toxocara larvae. A history of raw meat or liver consumption should cause one to suspect Toxocara. The clinical manifestations are diverse, which may present without granulomas, with normal central vision, and normal color vision in the early stages. Thus, toxocara IgG ELISA testing should be performed immediately in suspected cases for early diagnosis and treatment. Most patients in this series had vision loss following recurrences. Lastly, although atypical initially, most cases will eventually progress to the classic features of neuroretinitis. In conclusion, toxocara optic neuropathy should be considered in adults with optic disc swelling and a history of raw meat, specifically liver and blood products even without the typical features of ocular granuloma. Early diagnosis and treatment are invaluable to preserve the vision in patients with ocular toxocariasis.
ACKNOWLEDGMENTS Hee Kyung Yang and Se Joon Woo equally contributed to the work and therefore should be considered co-first authors. This work was supported by a Korea Science and Engineering Foundation (KOSEF) grant funded by the Korean government (MEST) (No. R01-2005000-10875-0). The authors have no proprietary interest in the manuscript. Received May 13, 2014; accepted July 29, 2014.
REFERENCES 1. Despommier D. Toxocariasis: clinical aspects, epidemiology, medical ecology, and molecular aspects. Clin Microbiol Rev 2003; 16:265Y72. 2. Woodhall D, Starr MC, Montgomery SP, Jones JL, Lum F, Read RW, Moorthy RS. Ocular toxocariasis: epidemiologic, anatomic, and therapeutic variations based on a survey of ophthalmic subspecialists. Ophthalmology 2012;119:1211Y7. 3. Komiyama A, Hasegawa O, Nakamura S, Ohno S, Kondo K. Optic neuritis in cerebral toxocariasis. J Neurol Neurosurg Psychiatry 1995;59:197Y8. 4. Phillips CI, Mackenzie AD. Toxocara larval papillitis. Br Med J 1973;1:154Y5. 5. Bird AC, Smith JL, Curtin VT. Nematode optic neuritis. Am J Ophthalmol 1970;69:72Y7. 6. Kim YJ, Moon CH, Chang JH. Toxocariasis of the optic disc. J Neuroophthalmol 2013;33:151Y2. 7. Cox TA, Haskins GE, Gangitano JL, Antonson DL. Bilateral Toxocara optic neuropathy. J Clin Neuroophthalmol 1983;3:267Y74. 8. Watthanakulpanich D. Diagnostic trends of human toxocariasis. J Trop Med Parasitol. 2010;33:44Y52. Available at: http://www.tm. mahidol.ac.th/tropmed-parasitology/2010-33-1/2010-33-1-e7.pdf. Accessed August 26, 2014. 9. Stewart JM, Cubillan LD, Cunningham ET, Jr. Prevalence, clinical features, and causes of vision loss among patients with ocular toxocariasis. Retina 2005;25:1005Y13. 10. Glickman LT, Schantz PM. Epidemiology and pathogenesis of zoonotic toxocariasis. Epidemiol Rev 1981;3:230Y50. 11. Yoshida M, Shirao Y, Asai H, Nagase H, Nakamura H, Okazawa T, Kondo K, Takayanagi TH, Fujita K, Akao N. A retrospective study
Optometry and Vision Science, Vol. 91, No. 11, November 2014
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Toxocara Optic Neuropathy after Ingestion of Raw MeatVYang et al.
12.
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of ocular toxocariasis in Japan: correlation with antibody prevalence and ophthalmological findings of patients with uveitis. J Helminthol 1999;73:357Y61. Ahn SJ, Woo SJ, Jin Y, Chang YS, Kim TW, Ahn J, Heo JW, Yu HG, Chung H, Park KH, Hong ST. Clinical features and course of ocular toxocariasis in adults. PLoS Negl Trop Dis 2014;8:e2938. Lee AG, Beaver HA. Acute bilateral optic disk edema with a macular star figure in a 12-year-old girl. Surv Ophthalmol 2002;47:42Y9. Cortez RT, Ramirez G, Collet L, Giuliari GP. Ocular parasitic diseases: a review on toxocariasis and diffuse unilateral subacute neuroretinitis. J Pediatr Ophthalmol Strabismus 2011;48:204Y12. Smith H, Holland C, Taylor M, Magnaval JF, Schantz P, Maizels R. How common is human toxocariasis? Towards standardizing our knowledge. Trends in Parasitology 2009;25:182Y8. Schantz PM, Weis PE, Pollard ZF, White MC. Risk factors for toxocaral ocular larva migrans: a case-control study. Am J Public Health 1980;70:1269Y72. Schneier AJ, Durand ML. Ocular toxocariasis: advances in diagnosis and treatment. Int Ophthalmol Clin 2011;51:135Y44. Hayashi E, Akao N, Fujita K. Evidence for the involvement of the optic nerve as a migration route for larvae in ocular toxocariasis of Mongolian gerbils. J Helminthol 2003;77:311Y5.
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19. Rathinam SR, Annamalai R, Biswas J. Intraocular parasitic infections. Ocul Immunol Inflamm 2011;19:327Y36. 20. Girdwood RW, Smith HV, Bruce RG, Quinn R. Human Toxocara infection in west of Scotland. Lancet 1978;1:1318. 21. Jin Y, Shen C, Huh S, Sohn WM, Choi MH, Hong ST. Serodiagnosis of toxocariasis by ELISA using crude antigen of Toxocara canis larvae. Korean J Parasitol 2013;51:433Y9. 22. Kim YH, Huh S, Chung YB. Seroprevalence of toxocariasis among healthy people with eosinophilia. Korean J Parasitol 2008;46:29Y32. 23. Yang JH, Kim M, Kim ES, Na BK, Yu SY, Kwak HW. Imported intraocular gnathostomiasis with subretinal tracks confirmed by western blot assay. Korean J Parasitol 2012;50:73Y8.
Jeong-Min Hwang Department of Ophthalmology Seoul National University College of Medicine Seoul National University Bundang Hospital 300 Gumi-dong, Bundang-gu Seongnam, Gyeonggi-do 463-707 Korea e-mail: [email protected]
Optometry and Vision Science, Vol. 91, No. 11, November 2014
Copyright © American Academy of Optometry. Unauthorized reproduction of this article is prohibited.
CLINICAL CASE
Toxocara Optic Neuropathy after Ingestion of Raw Meat Products Hee Kyung Yang*, Se Joon Woo*, and Jeong-Min Hwang*
ABSTRACT Purpose. To report Toxocara optic neuropathy in five men with histories of ingestion of raw meat, liver, or blood. Case Report. Five men in their 30s to 60s presented with unilateral visual disturbance. All five had a history of ingesting raw meat, liver, or blood products. All five men presented with optic disc edema and three also showed granulomatous infiltration of the retina. With Goldmann or Humphrey visual field testing, two patients showed central scotomas and two exhibited arcuate defects. Serum eosinophil count and total IgE were elevated in four patients. Serum enzyme-linked immunosorbent assay testing was positive for Toxocara canis IgG in all five cases. Conclusions. This report shows the variable clinical presentations of Toxocara optic neuropathy and the importance of questioning for a history of eating raw meat and blood products as a risk factor. (Optom Vis Sci 2014;91:e267Ye273) Key Words: Toxocara optic neuropathy, raw meat, ocular toxocariasis, toxocariasis, neuroretinitis
T
oxocariasis is a nematode infection by Toxocara canis or Toxocara cati.1Y22 Domesticated cats and dogs are the usual primary host and humans are infected mainly through the ingestion of Toxocara eggs in soil contaminated by dog and cat feces.1,2 Children are at risk of infection by eating dirt or frequent contact with puppies; thus, it has been reported that toxocariasis mainly affects children.1,2 On the other hand, raw meat products are also easily contaminated with embryonated helminthic eggs. There are many situations for adults to consume raw meat as a variety of cultural foods, such as Parisa (South Texas), Carne Apache (Mexico), Crudos (Chile), Mett (Germany), Steak tartare (France), Basashi (Japan), Ossenworst (The Netherlands), Beef Carpaccio (Italy), Asbeh nayeh (Lebanon), Yookhwe (Korea), Koi Soi (Thailand), or Bo Tai Chanh (Vietnam), which may also be the route for Toxocara infection. The most common ophthalmic sign of ocular toxocariasis is subretinal granulomas involving the macula and peripheral retina.1Y12 Although there are a few case reports of toxocariasis involving the optic nerve in the literature,3Y7 there has not been a published case series. The purpose of this case series was to report different histories and clinical manifestations of
*MD Department of Ophthalmology, Seoul National University College of Medicine, Seoul National University Bundang Hospital, Seongnam, Korea (all authors).
toxocara optic neuropathy. All cases showed unilateral optic nerve involvement.
CASE REPORTS Case 1 A 31-year-old man presented with sudden visual blurring and pain on eye movement in the right eye (OD) (Table 1). He had a pet dog and frequently ate raw minced beef and raw cow liver. His visual acuity was 20/200 OD. Fundus examination showed edema and whitish infiltration of the optic disc with subtle vitritis OD (Fig. 1). Optical coherence tomography showed a white intraretinal lesion near the disc protruding from the retinal surface into the vitreous (Fig. 2). Goldmann perimetry showed a large central scotoma. Hardy, Rand, and Rittler (HRR) color vision testing showed a strong blue-yellow defect. Systemic underlying causes of unilateral disc edema including autoimmune diseases, inflammatory conditions, cancer masquerade syndromes, and infectious etiologies were considered. The results of an extensive serology and microbiological screening, including complete blood count; erythrocyte sedimentation rate; C-reactive protein; antiYdouble-stranded DNA antibodies; rheumatoid factor; complement components; anticardiolipin antibodies; angiotensin-converting enzyme; antineutrophil cytoplasmic antibodies; and immunoglobulins (Ig) G, A, and M; were unremarkable. Microbiological tests were negative
Optometry and Vision Science, Vol. 91, No. 11, November 2014
Copyright © American Academy of Optometry. Unauthorized reproduction of this article is prohibited.
e268 Toxocara Optic Neuropathy after Ingestion of Raw MeatVYang et al. TABLE 1.
Demographics and clinical findings of five patients Patient no. 1
2
3
4
5
Male 36 R Raw cow liver, minced beef j Sudden visual loss
Male 68 R Raw cow stomach, liver, minced beef j Sudden visual loss
Male 45 L Raw cow liver, deer blood j Sudden visual loss
Ocular pain Initial VA Final VA Visual field
Male 31 R Raw cow liver, minced beef Dog Progressive visual loss + 20/200 FC Central scotoma
j 20/800 20/50 Central scotoma
j 20/800 20/40 Not done
Color vision Granuloma Disc edema Additional features
Strong BY defect + ++ Circumpapillary choroidal folds
Achromatopsia + + Macular edema and exudate
Not done + + Macular edema and exudate
+ 20/100 20/30 Inferior arcuate scotoma Normal j + Macular edema and exudate
0.512 5.8
0.444 6.8
0.463 5.6
1.676 6.8
Male 49 R Raw liver of cow and rabbit Y Inferotemporal visual field defect + 20/20 20/100 Superior and inferior arcuate scotoma Normal + ++ Circumpapillary choroidal folds, macular edema/exudate 1.380 3.2
415.3 Oral prednisolone, vitrectomy, later albendazole
338.6 Oral prednisolone, vitrectomy, later albendazole
104.3 Oral prednisolone, later albendazole
20.03 Oral prednisolone, later albendazole
+ 16
+ 31
862.1 Oral prednisolone, early albendazole, intravitreal bevacizumab j 26
+ 4
+ 9
Epiretinal membrane, temporal pallor
Epiretinal membrane, temporal pallor
Mild temporal pallor, no granuloma
Temporal pallor, dot hard exudates
Temporal pallor, dot hard exudates
Sex Age, y Affected eyes History of raw food Pet Symptom
T. canis IgG titer* Eosinophil counts, %† Total IgE, IU/mL‡ Treatment
Recurrence Duration of follow-up, mo Final fundus findings
*Normal range, 0 to 0.250 optical densities.13 †Normal range, 1 to 5%. ‡Normal range, 0 to 100 IU/mL. VA, visual acuity; FC, finger count; BY, blue yellow.
for syphilis, Lyme disease, interferon-F release assay, toxoplasmosis, bartonella, herpes simplex virus, varizella zoster virus, and HIV. After high-dose steroid therapy, visual acuity recovered to 20/20 OD and optic disc edema resolved, leaving a granulomatous infiltration on the optic disc and lipid exudates within the macula. However, after steroid tapering, vision decreased to counting fingers and new severe vitritis with retinal granulomatous lesions involving the macula were seen (Fig. 1). He underwent pars plana vitrectomy; however, ocular inflammation waxed and waned with the use of systemic steroids. At that time, we performed additional microbiological testing and serum enzyme-linked immunosorbent assay (ELISA) titers were positive for T. canis IgG. Serum eosinophil count was slightly elevated, and total IgE levels were increased. Administration of oral albendazole 400 mg bid for 2 weeks was followed with a tapered dose of continuous steroid therapy (initial dose of 0.5 mg/kg
per day). After treatment, the inflammation was well controlled without significant recurrence. However, because of scar tissue formation involving the fovea, his visual acuity remained counting fingers.
Case 2 A 36-year-old man presented with sudden visual loss that developed 4 days prior without ocular pain OD. He did not have a pet and used to eat raw cow liver and minced beef. His visual acuity was 20/800 OD. Fundus examination revealed disc edema and whitish infiltration of the optic disc with retinal hemorrhage and exudates involving the macula (Fig. 1). Optical coherence tomography showed a white intraretinal granulomatous lesion (Fig. 2). Goldmann perimetry showed a large central and inferior scotoma. He did not pass any of the color plates of the HRR test and could only recognize the screening plate
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Toxocara Optic Neuropathy after Ingestion of Raw MeatVYang et al.
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FIGURE 1. Fundus photographs at initial presentation before treatment and 1 to 2 months later. Cases 1 to 3 showed optic disc edema and granulomas of the peripapillary retina. Cases 4 and 5 showed optic disc edema without granuloma at initial presentation, but vitritis and macular exudates eventually developed. Granulomas newly appeared in case 5. Optometry and Vision Science, Vol. 91, No. 11, November 2014
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e270 Toxocara Optic Neuropathy after Ingestion of Raw MeatVYang et al.
FIGURE 2. Optical coherence tomography. Cases 1 to 3 showed optic disc edema with whitish granulomatous lesions (arrows) on the disc or peripapillary retina. Cases 4 and 5 showed optic disc edema without any demonstrable lesion of granuloma at initial presentation. However, granulomas newly developed in case 5 (arrow).
of the Ishihara color vision test. Ocular inflammation subsided with the use of oral prednisolone. Two months later, vitritis, macular exudates, and new granulomatous lesions in the macula developed. He underwent pars plana vitrectomy and the ocular inflammation waxed and waned with the use of systemic steroids. An extensive laboratory screening panel showed negative results except for positive serum ELISA titers for T. canis IgG and elevated serum eosinophil counts and total IgE levels. Administration of oral albendazole 400 mg bid for 2 weeks was followed with a tapered dose of continuous steroid therapy. His visual acuity was limited to 20/50 because of scar tissue formation and photoreceptor disruption in the macula.
Case 3 A 68-year-old man presented with sudden visual loss that developed 1 week prior without ocular pain OD. He did not have a pet and used to eat raw cow stomach, liver, and minced beef. His visual acuity was 20/800 OD. Visual field and color vision testing were not performed. Fundus examination revealed disc edema with peripapillary whitish infiltration and subretinal fluid accumulation that involved the macula OD (Fig. 1). Optical coherence tomography showed a peripapillary intraretinal granulomatous lesion (Fig. 2). Serum ELISA titers were positive for T. canis IgG. Serum eosinophil count and total IgE levels were increased. A month after treatment with albendazole 400 mg bid for 2 weeks
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Toxocara Optic Neuropathy after Ingestion of Raw MeatVYang et al.
and oral prednisolone, optic disc and macular edema decreased, leaving exudates within the macula. The patient was followed for 26 months without recurrence. Visual acuity remained 20/25 (Fig. 1).
Case 4 A 45-year-old man presented with visual blurring that developed 2 weeks prior preceded by ocular pain in the left eye (OS). He used to eat raw cow liver and deer blood. His visual acuity was 20/100 OS. Fundus examination revealed optic disc edema and hemorrhage without granulomas within the retina OS (Fig. 1). Optical coherence tomography showed no demonstrable granulomatous lesions of the optic disc or macula OS (Fig. 2). Humphrey visual fields showed an inferior arcuate scotoma OS. Results of HRR color vision testing were normal. An initial diagnosis of nonarteritic anterior ischemic optic neuropathy was made and systemic steroids were applied for 5 days. One month later, his visual acuity had decreased to 20/100 and star-shaped retinal exudation in the macula had developed OS. An extensive laboratory screening panel showed negative results except for positive serum ELISA titers for T. canis IgG and increased serum eosinophil counts and total IgE levels. Administration of oral albendazole 400 mg bid for 2 weeks was followed with a tapered dose of continuous steroid therapy. After treatment, the inflammation gradually subsided and visual acuity improved to 20/30.
Case 5 A 49-year-old man presented with inferotemporal visual field defects for 3 to 4 days OD. He ate raw cow and rabbit liver about 6 months prior. Visual acuity was 20/20 and fundus examination showed disc edema, circumpapillary choroidal folds, and dilated tortuous retinal veins OD (Fig. 1). Optical coherence tomography showed no demonstrable granulomatous lesions of the optic nerve or retina. Humphrey visual fields showed arcuate scotomas inferiorly greater than superiorly. The results of the HRR color vision testing were normal. An initial diagnosis of nonarteritic anterior ischemic optic neuropathy was made and systemic steroids were applied for 5 days. Two weeks later, his vision deteriorated to hand motion in the right eye as an optic disc granuloma with macular-star pattern exudates developed (Fig. 1). Optical coherence tomography showed whitish intraretinal lesions near the optic disc and macular subretinal fluid (Fig. 2). An extensive laboratory screening panel was nondiagnostic except for positive serum ELISA titers for T. canis IgG and increased total IgE levels. Serum eosinophil counts were normal. Administration of oral albendazole 400 mg bid for 2 weeks was followed with a tapered dose of steroid therapy. After the treatment, the inflammation subsided without recurrence during 10 months of follow-up. His vision improved to 20/100 with a remnant cecocentral scotoma on perimetry.
DISCUSSION This report represents the largest series of patients with toxocara affecting the optic nerve. The patients were all men in their 30s to 60s who had a history of eating raw meat, liver, or animal blood.
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Domesticated cats and dogs are the usual primary host, but only case 1 had a pet dog. Three of five patients had sudden visual loss. Three of five patients had ocular pain. Four out of five patients presented with loss of their central vision, ranging from 20/100 to 20/800. The fifth patient presented with peripheral visual field loss. Fundus findings included subtle to severe optic disc swelling in all patients, retinal granulomas at initial presentation in three patients, and two delayed onset retinal granulomas after a few weeks. There were circumpapillary choroidal folds in two patients, and eventually all five patients manifested macular exudates. Color vision varied from normal to total achromatopsia. Visual field testing showed central scotomas in two patients and arcuate scotomas in two other patients. Serum ELISA titers were positive for T. canis IgG in all patients. Four of five patients showed elevated eosinophil counts and total IgE antibodies. At presentation, case 2 showed disc edema accompanied by star-patterned macular exudates as did cases 4 and 5 later in their courses. Besides toxocara, this clinical picture can be seen with increased intracranial pressure and ischemic optic neuropathies. Malignant hypertensive retinopathy and central retinal vein occlusion can also result in disc edema with associated macular exudates as can neuroretinitis caused by inflammatory or infectious etiologies. In the presented case series, this list of differentials could be narrowed down based on the clinical presentation and with the appropriate laboratory investigations. Malignant hypertensive retinopathy and increased intracranial pressure usually result in bilateral disc swelling and may be accompanied by symptoms of headache, transient visual obscuration, or pulsatile tinnitus. Hypertensive retinopathy and central retinal vein occlusion usually also manifest with more widespread intraretinal hemorrhages as well as retinal vessel caliber or crossing changes. None of these findings were seen in these cases and none of the patients had increased blood pressure at the time of examination. The infectious and inflammatory causes of neuroretinitis should also be ruled out as part of the laboratory work-up for disc swelling associated with macular exudation. Causative viral agents include mumps, Epstein-Barr virus, HIV, herpes simplex virus, and hepatitis B and C viruses. Although cultures from the vitreous humor, aqueous humor, or cerebral spinal fluid are possible, positive cultures are rare. Other nonviral infectious causes include Bartonella henselae (cat scratch disease), Toxoplasma gondii (toxoplasmosis), Treponema pallidum (syphilis), Leptospira spp. (leptospirosis), Borrelia burgdorferi (Lyme disease), Mycobacterium tuberculosis (tuberculosis), Rickettsia typhi (murine typhus), Brucella spp. (brucellosis), and Histoplasma capsulatum (histoplasmosis). Clinical history is also important when neuroretinitis is suspected. The diagnosis of Lyme disease may be aided by a history of tick bite, cutaneous rash, or migrating musculoskeletal pain. Questions regarding contact with cats should be pursued for cat scratch disease and a thorough sexual history should be taken for risk of syphilitic infection. Rarely, ocular toxocariasis can be definitively diagnosed by direct observation of the larva in the eye. More often, it is diagnosed with a combination of positive serology and clinically observed granulomas of the retina or optic nerve. Detection of serum antitoxocara IgG with an indirect ELISA on the Toxocara larva antigen is diagnostic. Elevated eosinophil counts could also be helpful for the diagnosis of helminthic infection if present.
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e272 Toxocara Optic Neuropathy after Ingestion of Raw MeatVYang et al.
However, eosinophil counts could be normal or only mildly elevated with ocular toxocariasis. Cases 4 and 5 were unique in that they showed only disc swelling without granulomas at their initial presentation. Their initial visual acuities of 20/100 and 20/20, respectively, were also better than the other cases. Color vision was normal with only arcuate scotomas seen on visual field testing. This mild presentation may represent the early stage of toxocara optic neuropathy and mimics more common optic neuropathies such as anterior ischemic optic neuropathy. Hayashi et al.18 showed that the optic nerve could be a migratory route of T. canis from the brain to the eye in an animal model of Mongolian gerbils. Therefore, cases 4 and 5 may represent the clinical presentation as the T. canis is migrating within the nerve before development of the classic granulomatous response. Therefore, careful follow-up examination over time is mandatory in suspected patients. Based on the observations from this case series, a history of ingesting raw meat or blood products should also raise the suspicion of ocular toxocariasis. Because ocular toxocariasis is relatively rare, suspicion of it as a diagnosis usually requires a typical clinical presentation. Thus, in the absence of visible granuloma, it is difficult to suspect toxocara as the etiology of the optic neuropathy and the diagnosis is dependent on positive serologic tests. Based on the reported cases, toxocara optic neuropathy may be differentiated from other acute optic neuropathies in the following ways: (1) presence of granulomas of the optic nerve or retina, (2) peripapillary subretinal exudation and localized serous retinal detachment, (3) positive serum toxocara IgG assay, (4) history of ingestion of raw meat, and (5) recurrence with vitritis. The preferred management of ocular toxocariasis has not been settled. Corticosteroid is the mainstay for treatment, reducing the inflammatory response and preventing the development of tractional retinal detachment.14,15 Oral prednisolone 1 mg/kg daily for 1 month or more is commonly prescribed. The need for antihelminthics is controversial because of the concern that dead larvae can cause more severe reaction and permanently damage the eye.16 However, Ahn et al.12 found that combined treatment of albendazole (400 mg twice a day for 2 weeks) and oral prednisolone (0.5 to 1 mg/kg per day) significantly lowered the 6-month recurrence rate compared with corticosteroid monotherapy. Albendazole is the drug of choice because it crosses the blood-brain and blood-retina barriers.17 In addition to toxocariasis, raw meat ingestion could result in other intraocular parasitic infections such as gnathostomiasis, toxoplasmosis, cysticercosis, onchocerciasis, and ophthalmomyiasis.19,20 Therefore, patients with any suspicious lesions should be asked about raw meat ingestion. Based on the patient histories taken from the presented case series, no definitive conclusions could be drawn regarding timing of ingestion of the raw meat or blood products and when the eye became involved. Because ingestion of such food likely was a regular part of their diets, only one of the reported patients (case 4) could remember that he had ingested raw cow liver and deer blood specifically 6 months prior. A previous report also demonstrated a patient who developed intraocular gnathostomiasis after ingestion of raw wild boar meat and lobster 8 months prior.23 Toxocara larvae can survive in human tissues over 10 years; therefore, any ingestion up to 10 years can cause ocular toxocariasis.20
There are several important messages from this case series. Although toxocariasis is typically considered a childhood disease, it can affect any age group that ingests toxocara larvae. A history of raw meat or liver consumption should cause one to suspect Toxocara. The clinical manifestations are diverse, which may present without granulomas, with normal central vision, and normal color vision in the early stages. Thus, toxocara IgG ELISA testing should be performed immediately in suspected cases for early diagnosis and treatment. Most patients in this series had vision loss following recurrences. Lastly, although atypical initially, most cases will eventually progress to the classic features of neuroretinitis. In conclusion, toxocara optic neuropathy should be considered in adults with optic disc swelling and a history of raw meat, specifically liver and blood products even without the typical features of ocular granuloma. Early diagnosis and treatment are invaluable to preserve the vision in patients with ocular toxocariasis.
ACKNOWLEDGMENTS Hee Kyung Yang and Se Joon Woo equally contributed to the work and therefore should be considered co-first authors. This work was supported by a Korea Science and Engineering Foundation (KOSEF) grant funded by the Korean government (MEST) (No. R01-2005000-10875-0). The authors have no proprietary interest in the manuscript. Received May 13, 2014; accepted July 29, 2014.
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Jeong-Min Hwang Department of Ophthalmology Seoul National University College of Medicine Seoul National University Bundang Hospital 300 Gumi-dong, Bundang-gu Seongnam, Gyeonggi-do 463-707 Korea e-mail: [email protected]
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