Continuing Education Activity

Ocular toxocariasis is a childhood disorder resulting from the ingestion of Toxocara ova. The patient may present with peripheral granuloma, posterior granuloma, or endophthalmitis. It is a serious ocular condition causing permanent vision loss, and it is an important differential diagnosis of retinoblastoma. It must be promptly diagnosed and treated after excluding other differential diagnoses to avoid the high morbidity associated with ocular toxocariasis. This activity reviews the evaluation and treatment of ocular toxocariasis and highlights the role of the interprofessional team in evaluating and treating patients with this condition.

Objectives:

• Describe the pathophysiology of ocular toxocariasis.
• Summarize the typical presentation/examination findings of a patient with ocular toxocariasis.
• Explain the appropriate treatment of ocular toxocariasis.
• Describe the common complications, differential diagnoses, and role of interprofessional approach for patients with ocular toxocariasis.

Introduction

Helminths have been causing disease in human beings for since long.[1] Helminths are divided into phylum, Nemathelminthes, and Platyhelminths. Nematodes are a class of Nemathelminthes that include human worms (Ascaris lumbricoides, Trichuris trichiura), animal worms (Toxocara canis, Toxocara catis), and filarial worms (Wuchereria bancrofti). Platyhelminths are divided into trematodes (Schistosoma mansoni) and cestodes (Taenia solium). Worldwide around 1 billion people are infected with helminths.[2]

They are pathogenic to humans. They parasitize the intestine and cause tissue damage by direct invasion. Ocular toxocariasis is a zoonotic infection. It is caused by the nematode Toxocara canis and Toxocara cati.[3] In 1950, Wilder described the ocular infection caused by a nematode.[4] She studied 46 enucleated eye specimens and found nematode larva in 24 of them. Beaver, in 1952, identified the Toxocara larva in the liver biopsies of children.[5] Nichols in 1956 demonstrated T. canis in 24 enucleated eye specimens.[6]

These findings implicated Toxocara as a common etiology for systemic and ocular pathology. Ocular toxocariasis may present with peripheral granuloma, posterior granuloma, or endophthalmitis. This review discusses etiology, epidemiology, pathophysiology, clinical features, investigations, differential diagnoses, management, complications, and the role of interprofessional coordination for patients with ocular toxocariasis.

Etiology

Ocular toxocariasis is caused by Toxocara. The Toxocara genus consists of 21 species.[7] Toxocara canis species is the most common cause of toxocariasis.[8] It is a natural parasite of dogs. The adult worms are cylindrical. The length of adult male worms is 42.5 to 45 mm, and female worms are usually 54 to 60 mm long.[9]

Puppies are the definitive host.[7] Adult worms are found in the small intestine of puppies and pregnant dogs. The puppies get infected either through maternal transmission or through ingestion of contaminated soil and feces. Inside them, the larva reaches the lungs. These larvae are coughed up and swallowed. They then reach the small intestine and quickly mature into adult worms that produce infectious ova. These eggs are shed in the feces.[10] 

The eggs mature into an embryo in 2-6 weeks in the external environment. Humans get infected through the ingestion of contaminated soil or contaminated food. The embryo reaches the intestine and matures into a larva. The larva penetrates the intestinal wall and enters the systemic circulation. It is then carried to various organs like the heart, liver, lungs, and eyes.[11]

Epidemiology

Ocular toxocariasis is widespread around the world. According to the National Health and Nutrition Examination Survey (NHANES, 1988-1994), 13.9% of the US population was seropositive for Toxocara. But the recent NHANES (2011-2014) data reported 5.1% seropositivity.[12] Seropositivity was higher in blacks than whites.[13] It is prevalent in warmer areas such as the Southern United States.[14] According to a study, 45% of Toxocara patients belonged to this region.

In other parts of the world, the antibody titer against Toxocara was found to be positive in 2.4% to 76.6% of individuals.[15] Seroprevalence above 80% was reported among the children in some regions of Nigeria.[16] It is generally seen in the younger population. The median age of infection is 11.5 years (1 to 66 years).[17] The majority of them are male. According to a study, 69% of patients had a history of contact with a dog or a cat, 85% reported vision loss, and 70% had permanent vision loss.[18]

Pathophysiology

Humans get infected after ingestion of eggs or larvae through contaminated vegetables or uncooked meat. Close contact with puppies or soil infested with embryonated eggs can lead to accidental ingestion of eggs.[19][20] The perianal region of dogs is a reservoir of embryonated eggs. The dogs also harbor the eggs in their fur. According to a study, puppies harbor many eggs on their hair at densities higher than in the soil.[21] Thus direct contact with puppies can lead to infection of T. canis.[22] Sometimes people get infected after consumption of uncooked contaminated raw meat of chicken and cows.[23][24] After ingestion, the eggs reach the small intestine. There they turn into larva. The larva penetrates the intestinal wall and enters the systemic circulation. 

The body tries to contain the infection by inciting an eosinophilic granuloma around the parasite.[25] It tries to contain the Toxocara parasite within the granuloma. Toxocariasis can manifest in the form of visceral larva migrans and ocular toxocariasis. The clinical manifestation depends upon host immunity, the severity of inflammatory response, the quantity of larva ingested, and organ localization.[26] Eosinophilia is often present in Toxocara infection. The greater the degree of exposure greater is the eosinophil count.[27]

Histopathology

The eosinophilic granulomas are often multiple, with central necrosis surrounded by eosinophils, neutrophils, lymphocytes, epithelioid histiocytes, and/or giant cells. They are present predominantly around the blood vessels. Charcot-Leyden crystals are often present. Remnants of parasites might be present in some cases. Serologic test for Toxocara may be positive. Immunohistochemical staining using polyclonal antisera against Toxocara larvae demonstrates positivity in macrophages in sixty percent of cases.[25]

History and Physical

Ocular toxocariasis generally affects young children. A history of close contact with a dog, cat, or soil contamination is usually present. The average age of presentation is eight years.[28] It is generally not seen in adults and very young children.[29]

Most of the time, the children do not complain. The parents notice ocular changes, including a deviation of the eye (squinting), white (leukocoria), and redness. Children may present with unilateral loss of vision, redness, and pain. Vision may range from 20/80 to perception of light (PL).[30][31][32] The slit-lamp evaluation may reveal anterior chamber cells, flare, cataract, and retrolental cells.[33] 

Retinal findings can manifest in 3 forms. The patient can present with any manifestation.

1. Peripheral granuloma presents as an elevated white mass in the periphery with surrounding vitreal membranes, pigmentation, and tractional detachment. The usual age of onset is 6 to 40 years. A fold of membrane may extend from the peripheral granuloma to the posterior pole.[34][35] This traction band can cause macular displacement and optic neuropathy. Generally, there is no vitritis.[31] The prognosis is usually good. Children present with unilateral leukocoria, vision loss, or squint. A very young child may not present as the disease is peripheral and visual acuity is good.[34] It is most commonly found incidentally after an ophthalmic examination. Adults present with unilateral loss of vision.[36]
2. Posterior granuloma presents as a solitary elevated yellow-white mass at the posterior pole (at macula or around the optic disc) ranging from 0.5 to 3 disc diameter. The patients are usually 6 to 14 years old. Usually, the intraocular inflammation is absent or minimal. Generally, it is well defined and lies in the subretinal space.[37] But when the disease is active, it appears as an ill-defined mass with surrounding exudates and hemorrhage.[34] Traction bands may form in between the granuloma and the surrounding retina. Vision loss occurs by macular or optic disc involvement, epiretinal membranes, retinal folds, or choroidal neovascularization.[34] 
3. Endophthalmitis: The usual age at presentation is 2 to 9 years. Patients present with signs of severe inflammation, pain, redness, watering, and photophobia.[20][38] There is intense vitritis that may preclude posterior segment visualization. The slit-lamp examination shows flare and cells in the anterior chamber. The intraocular pressure may be lower than normal. Peripheral granuloma or grayish-white exudates may be hazily seen near the pars plana.

The diagnosis of ocular Toxocara is mainly clinical, supported by antibody testing to Toxocara. The disease, if untreated, can cause complications like cataracts, glaucoma, tractional retinal detachment, macular scarring, and phthisis bulbi.[26][39][40]

Evaluation

Ocular toxocariasis is suspected if a child presents with unilateral loss of vision or squint. Definitive diagnosis is made by the demonstration of Toxocara larva in the histological sections of the affected tissue.[41] In ocular infection, the retinal biopsy is not feasible, so this test is rarely performed.[42][43] Thus the diagnosis is mainly clinical and presumed most of the time without histopathology or other direct confirmation.[44] When in doubt, as in cases presenting with endophthalmitis, ultrasonography (USG) B scan or computed tomography (CT) scan can be done.

USG shows a hyperreflective retinal mass located in the posterior pole or periphery. Often, vitreous membranes are noted to be adherent to the mass with or without calcification.[45] If calcification is present, it is focal and limited and does not involve the whole vitreous as in retinoblastoma.[46] The fibrous band extending from the periphery to the posterior pole or optic disc may also be demonstrated. In a healed peripheral and posterior pole granuloma, a CT scan shows a focal or diffuse, non-enhancing, well-defined hyperdense lesion.[47] 

Immunological tests can be done for the diagnosis of toxocariasis. The enzyme-linked immunosorbent assay (ELISA) test, which employs antigens of the second-stage larva (usually excretory/secretory antigens), is the best indirect test for diagnosing the infection. It is a qualitative immunoenzymatic determination of antibodies against the Toxocara. ELISA may show cross-reactivity with Ascaris lumbricoides which can be minimized by using excretory/secretory antigens for the assay. ELISA has a high degree of sensitivity (78%) and specificity (92%) at a titer of more than 1:32.[48] However, serum ELISA may be negative in ocular toxocariasis.[49] ELISA on the aqueous and vitreous aspirate may improve the rate of detection. Positive ELISA reports may be noted in patients with past infections or asymptomatic Toxocara infection. A significant rise in antibody level over time confirms active infection.

Complete blood count may show eosinophilia.[50] Other indirect indicators are hypergammaglobulinemia (IgM) and an elevated isohemagglutinin titer. In humans, the intestinal form of toxocariasis does not occur, so stool studies for parasites and ova may not be helpful.[51] Tissue biopsy may show a granuloma surrounding a larva but is rarely recommended. Thus, the constellation of clinical signs described above, a history of pets, pica, eosinophilia, and positive serology, strongly point to the diagnosis. 

Serum total immunoglobulin-E (IgE) level may be markedly raised in patients with toxocariasis, though the titer may be lower in ocular toxocariasis due to reduced worm burden.

Treatment / Management

Ocular toxocariasis can present with or without active inflammation. In cases with anterior chamber cells/flare and vitritis, the inflammation must be controlled with topical and systemic corticosteroids. This helps in reducing anterior chamber reaction, vitreous haze, and vitreous membranes.[52]

Topical cycloplegic mydriatic prevents posterior synechia formation and seclusio pupillae. Increased intraocular pressure can be controlled with topical antiglaucoma medications. The role of systemic anthelmintic drugs such as albendazole and thiabendazole is unclear. It is not proven to kill intraocular Toxocara.[53][54] Though some cases have been described in the literature showing favorable results in combination with oral corticosteroids.[55][56][57] 

In one study, treatment resulted in an improved vision in all patients. There were no recurrences of uveitis during the study period of 13.8 months. In adults, the dose of albendazole was 800 mg orally twice a day for two weeks with prednisolone at 1.5mg/kg tapered over three months. The children received 200 mg orally twice a day for two weeks with prednisolone at 1mg/kg.[58]

Sometimes, the larva is seen migrating in the subretinal space. It can then be destroyed with laser photocoagulation over and around it.[59][60] The laser can be done with a neodymium-doped yttrium aluminum garnet (Nd: YAG) frequency-doubled 532 nm green laser. The laser power can be in the range of 250 to 300 mW and 100 to 150 ms duration. The reaction should produce a white burn over the retina.[61] Secondary complications like choroidal neovascularization can be treated with intravitreal anti-vascular endothelium growth factor agents.[62] 

Some patients present late without active inflammation. There is a peripheral focal granuloma with a vitreal fold radiating from it to the posterior pole. There can be accompanying tractional retinal detachment and a cataract. In such cases, surgery is indicated. Lens aspiration with intraocular lens implantation is preferred for the cataract. Pars plana vitrectomy is done for vitreous opacification and membranes.[63] It also relieves the traction bands and allows retinal reattachment. Epiretinal membrane over the macula and disc can be peeled off.[64] 

With such maneuvers, vision improves or remains stable in 85% of cases.[65] Sometimes a retinal tear occurs secondary to the traction from a peripheral granuloma. A scleral buckle can be placed to relieve the retinal traction and improve visual acuity.[30]

The most important step in the management of toxocariasis is prevention. Good hygiene should be maintained in children.[66] They should be prohibited from coming in close contact with dogs and cats. They should not play with contaminated soil and not walk bare feet outside. Meat should be properly cooked before consuming it. The puppies and dogs should be given anthelmintic drugs.[67] Their litter should be disposed of in plastic bags. Educating the parents and child about clean and hygienic habits is essential.

Differential Diagnosis

Differential diagnosis of toxocariasis includes retinoblastoma, endophthalmitis, retinopathy of prematurity (ROP), toxoplasmosis, panuveitis, Coats disease, persistent hyperplastic primary vitreous (PHPV), familial exudative vitreoretinopathy (FEVR), combined hamartoma of the retina, and retinal pigment epithelium (CHRRPE), and seasonal hyperacute panuveitis (SHAPU).[68][69]

Retinoblastoma is the most common intraocular malignancy of childhood.[59] It is generally diagnosed before three years of life which is a younger age group than that seen in toxocariasis. It presents with solid intraocular mass with calcification on the USG B scan. The tumor appears hyperechoic with irregular borders. The calcification is highly hyperechoic with back shadowing.[70]

Coats disease is generally seen in males. It is a unilateral condition and presents with retinal exudation, aneurysmal dilatation, telangiectasia, and occasional neovascularization.[71][69] Fluorescein angiography shows localized vascular anomalies (beading, telangiectasia, aneurysm) and peripheral non-perfusion.[72]

ROP usually presents within two months of birth.[73] There is a history of prematurity and/or low birth weight. It usually presents with peripheral retinal avascularity and a definite line or ridge with or without neovascularization.[74] In advanced cases (stages 4 and 5), retinal detachment may be noted.[75] So careful ultrasound is important to rule out peripheral and posterior pole granuloma.

PHPV is a congenital condition usually diagnosed in the first month of life. It presents with leukocoria, cataract, and a fibrovascular stalk extending from the optic disc to the posterior lens surface. The involved eye is usually microphthalmic with prominent ciliary processes.[76]

FEVR is a congenital condition that presents with straightening of the retinal vessel, retinal detachment, and peripheral avascular retina.[77] It is an autosomal dominant disorder with a positive family history.[78]

Endophthalmitis presents with lid edema, conjunctival congestion, discharge, hazy cornea, and vitreous exudates.[79]

Toxoplasmosis causes a focal necrotizing retinochoroiditis which appears as a yellowish elevated lesion at the posterior pole.[80] It usually reactivates at the edge of a scar which is often pigmented. There may be accompanying vitritis which gives the headlight in fog appearance.[81]

CHRRPE is a hamartomatous malformation involving the retina, retina pigment epithelium, and vitreoretinal interface.[82][83] It appears as a grey, elevated retinal lesion over the posterior pole with retinal vessel tortuosity and epiretinal membrane. On optical coherence tomography, it appears as a hyper-reflective retinal surface with underlying shadow due to the dense tissue and an epiretinal membrane.[83] Omega sign (omega-shaped appearance of inner retinal layers, the posterior margin of which is formed by the outer plexiform layer) has been recently described for this condition.[84]

SHAPU is a unilateral childhood ocular inflammatory disease reported only from Nepal since 1975. Initially, it occurred every two years, but recent reports have described it to occur annually during the summer or autumn months. It occurs suddenly in a healthy child. The child presents with complaints of sudden onset of redness, decreased vision, white pupillary reflex, and minimal pain. On examination, circumciliary congestion, fibrinous anterior chamber reaction, hypopyon, and shallow anterior chamber are present. The eyeball is soft (malignant hypotension). "White pupillary reflex in red-eye" and minimal pain is the hallmark of the disease. The cause is unknown though some studies have linked it to exposure to moths.[85] 

It is treated with injectable methylprednisolone for three days followed by oral steroids, topical antibiotics, steroids, and cycloplegic. Early core vitrectomy has shown promising results.[86] The prognosis is poor as two-thirds of patients present with blindness, and most of the rest lose vision rapidly.[87]

Prognosis

Patients presenting early in the course of the disease have a good prognosis.[88] The inflammation can be adequately controlled with oral corticosteroids and topical cycloplegic mydriatic.[58] This prevents vision loss and long-term complications.[89] Patients presenting late generally have guarded visual prognosis because of optic atrophy, macular changes, and retinal detachment.[90]

Complications

Prolonged inflammation leads to posterior synechia formation, which can cause iris bombe and angle-closure glaucoma.[29] Uncontrolled inflammation can cause ciliary body shutdown and hypotony.[91] Long-standing vitritis causes cystoid macular edema, epiretinal membrane, and macular degeneration.[66] Vitreal folds can cause tractional retinal detachment. Phthisis bulbi is the end stage of the disease.[92][40]

Deterrence and Patient Education

As ocular toxocariasis can cause permanent vision loss, preventative measures must be taken by the patients' families. The patients' family members should be adequately counseled regarding the prognosis of ocular toxocariasis and the importance of long-term follow-up.[93]

Enhancing Healthcare Team Outcomes

Any patient presenting with ocular toxocariasis should not only receive treatment by an ophthalmologist as it requires an interprofessional team evaluation by pediatricians and physicians. Interprofessional communication can lead to better patient management. The patient will most often present to the primary clinician, and these professionals should be aware of the condition as it is treatable.

Retinoblastoma is a close differential; therefore, prompt referral to an ophthalmologist is necessary. These patients can then be followed by their primary clinicians and should ensure compliance with treatment. The nursing staff will be the first to the department to come in contact with patients on follow-up. It can assess treatment progress, evaluate compliance with medication and lifestyle measures, and report any issues to the primary care clinician. This collaborative, interprofessional approach to care can ensure optimal patient outcomes.

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Disclosure: Abhishek Gupta declares no relevant financial relationships with ineligible companies.

Disclosure: Koushik Tripathy declares no relevant financial relationships with ineligible companies.