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Home , Cysticercosis, Onchocerca volvulus, Onchocerciasis, Retinitis, Taenia solium, Toxocara canis

Ophthalmol Clin N Am 15 (2002) 351–356

Nematode of the eye: , , diffuse unilateral subacute neuroretinitis, and

Nelson Alexandre Sabrosa, MD a,b,*, Moyse´s Zajdenweber, MD c,d

aDepartment of , University of Sa˜o Paulo, FMUSP, Sa˜o Paulo, bOphthalmology Department, Clı´nica Sa˜o Vicente, Rua Joao Borges, 204-Gavea, CEP 22451-100, Rio de Janeiro, Brazil cDepartment of Ophthalmology, Federal University of Sa˜o Paulo, Paulista School of Medicine, Sa˜o Paulo, Brazil dOphthalmology Department, Instituto Brasileiro de Oftalmologia, Praia de Botafogo 206, Botafogo, Rio de Janeiro, Brazil

Ocular toxocariasis may cause a large spectrum of illitis, each of which can lead to loss of vision in the manifestations in the eye, from an asymptomatic affected eye [7]. posterior , to total [1]. It represents one of the most common parasitic causes Epidemiology of visual loss throughout the world [2], and it usually affects young children. Other can cause Human toxocariasis is probably one of the most ocular disease, most of them related to adult large widespread zoonotic infections, occurring worms. Diffuse unilateral subacute neuroretinitis mainly in areas where the relationship between man, (DUSN) is a more recently described disorder soil, and is particularly close [8]. T canis is an believed to be caused by smaller nematodes [3,4]. often encountered canine parasite, affecting , Onchocerciasis and cysticercosis are seen mainly in , foxes, and other canidis, whereas T catis the developing world. may be found in domestic cats [9–11]. Human beings are contaminated through ingestion of the ova by geophagia, by eating contaminated foods, or by close Toxocariasis contact with puppies. Toxocariasis may manifest itself in the systemic form, visceral migrans, Wilder first recognized nematodes as pathogens in or the ocular form, ocular larva migrans. It is rare to the posterior segment of the eye in 1950. In 1952 see the ocular and visceral forms of the disease at the Beaver et al described the association of Toxocara same time. species with human disease [5]. Toxocariasis is a zoonotic disease caused by the of humans Ocular toxocariasis by second-stage larva of the dog nematode or the cat nematode T cati [6]. Ocular toxocar- Clinical features iasis may affect the eye causing , posterior and Toxocara is a well-documented cause of intra- peripheral retinochoroiditis, , or pap- ocular in children [11]. Clinical pre- sentation depends on the primary tissue or anatomic site of involvement, which may include the peripheral , the vitreous, the posterior pole, or the optic * Corresponding author. Ophthalmology Department, Clı´nica Sa˜o Vicente, Rua Joao Borges, 204-Gavea, CEP disk. The most common presentation involves peri- 22451-100, Rio de Janeiro, Brazil. pheral retina and vitreous, occurring separately or E-mail address: [email protected] together. A hazy white lesion may be seen or in the (N.A. Sabrosa). periphery, often with moderate vitreitis. As the

0896-1549/02/$ – see front matter D 2002, Elsevier Science (USA). All rights reserved. PII: S0896-1549(02)00024-X 352 N.A. Sabrosa, M. Zajdenweber / Ophthalmol Clin N Am 15 (2002) 351–356 inflammation resolves, a peripheral elevated white imaging techniques, such as ultrasonography, ultra- mass is seen better, and is typically associated with sound biomicroscopy, CT, or MRI studies, may be retinal folds extending toward the macula [12,13]. An helpful [5,14,15]. intraretinal or subretinal mass, or granuloma, is Treatment options for T canis depend on usually seen with the posterior form of disease. the type and severity of infection. Management of the Endophthalmitis, with mild or no anterior inflam- systemic form of toxocariasis includes the use of mation, is an uncommon but recognized presentation. systemic agents, antibiotics, or cortico- Papillitis can also occur, and it is usually caused by [7]. In patients with ocular toxocariasis, one an invasion of the by the nematode or as must have in mind the visual potential of the eye, the an inflammatory response to the organism in another amount of active inflammation, and the degree of site of the eye. The condition is almost always macular damage. In eyes with active vitreitis, sys- unilateral and it usually affects children, but also temic or periocular may represent an can be seen in adults [7]. important therapeutic tool. Anthelminthics may be used to destroy nematodes and eliminate further Pathogenesis and differential diagnosis migration of the larva, but the parasite may resist Sprent first described the T canis life cycle in 1958 such treatment. In some situations, such as to clear [5]. As mentioned previously, it is a canine round- vitreous debris, relieve vitreomacular traction, repair worm sharing certain characteristics with the feline tractional and tractional-rhegmatogenous retinal roundworm T catis and with the human roundworm detachments, and remove the posterior hyaloid, pos- [5]. Ingested Toxocara terior vitrectomy can be performed [16–18]. emerge in the . The larvae then perforate the intestinal wall, enter the circulation, and can lodge in the eye, most probably by the choroidal blood Onchocerciasis system. Thereafter the organism can migrate into the subretinal space or vitreous cavity, where it ultimately Onchocerciasis, also named river blindness or dies and is encapsulated by an eosinophilic granu- Robles disease, is a caused by the lomatous inflammatory reaction [4]. microfilariae volvulus [19]. O volvulus is a frequent finding in patients with is transmitted by the bite of the black ocular toxocariasis. The differential diagnosis includes , which breeds in rapidly flowing waters. The , endophthalmitis, of pre- clinical manifestations of onchocerciasis range from maturity, congenital , persistent hyperplasic no skin or eye lesions to very severe skin involvement primary vitreous, Coats’ disease, and various forms of and blindness. trauma [10,12,13].

Laboratory investigations and therapy Epidemiology and hypereosinophilia are present in most patients with . Eosino- Onchocerciasis is an disease in philia is usually absent in ocular toxocariasis. The and , but pockets of the disease also presence of larva can be disclosed by tissue , exist in . In Africa, the clinical and but because the are rarely able to finish their epidemiologic characteristics are different from other life cycle in humans, they are not detected on stool places. In the savannas, for example, about 40% of analysis. Until the use of the enzyme linked immu- the patients fewer than 40 years old develop blind- nosorbent assay (ELISA) test, immunodiagnostic ness [20]. Because of the high prevalence of this tests lacked sufficient sensitivity and specificity for disease in Africa it has become one of the main the diagnosis of ocular toxocariasis. In recent times, causes of blindness worldwide. According to the however, ELISA has become the main serologic World Health Organization, onchocerciasis affects at method for detecting visceral larva migrans, and for least 18 million people worldwide, and 300,000 are confirming the clinical suspicion of ocular toxocar- blind from the disease [21]. In Central America, the iasis. ELISA has a reported sensitivity of 78% and a clinical presentation seems to be the same, but ocular specificity of 92%, but it is known that the sensitivity involvement occurs earlier. In Brazil, for example, the and specificity of ELISA vary according to the cutoff disease occurs in the Yanomanis Indians in the north titer chosen defined as positive [14]. Most of the part of the country [22]. In this population, the ocular cases of ocular toxocariasis are diagnosed clinically, findings seem to be restricted to the and but in some patients with opaque media radiologic blindness tends not to occur [23]. N.A. Sabrosa, M. Zajdenweber / Ophthalmol Clin N Am 15 (2002) 351–356 353

Ocular features Epidemiology

The ocular manifestations of onchocerciasis are Initially described in the Southeastern and Mid- caused by the presence of dead parasites within the western parts of the United States and the Caribbean eye. The microfilariae penetrate the eye by the bulbar islands, DUSN has also been reported in other parts at the limbus, then invade the cornea, of North America, in South America, and in North- aqueous humor, and . They reach the posterior western Europe [29,30]. In Brazil DUSN is consid- segment by the circulation or ciliar nerves, which ered an important cause of posterior uveitis in supply the peripheral retina and . children and young healthy adults [34–37]. Puntate is often the first manifestation of onchocerciasis, the patient referring only to conjunc- Clinical features tival itching. The microfilariae then migrate to the cornea and eventually die causing a Because prompt treatment may prevent visual referred to as cracked-ice or snowstorm.Inlate loss, it is very important that the diagnosis of DUSN stages, the corneal lesions turn to scar tissue pro- be made early. Most patients with DUSN, however, ducing sclerosing keratitis as described by Pacheco- present with advanced disease. The onset is fre- Luna [24]. An iridocyclitis also can be seen and quently insidious, and patients usually complain of of the iris may occur. Other complications, unilateral paracentral or central , ocular dis- such as and , also may be present. comfort, or transient obscurations of vision [28]. Chorioretinal lesions typically begin in the periphery Patients are usually in good general health. The with pigmented lesions, sheating of the retinal ves- disease is characterized by unilateral vitreous inflam- sels, and visual field constriction. Optic atrophy tends mation, optic disk swelling, and the presence of to occur late in the disorder. Macular can also clusters of gray-white lesions in the deep retina. be found. DUSN is often misdiagnosed as multifocal choroid- itis, multiple evanescent white dot syndrome, acute posterior multifocal placoid pigment epitheliopathy, Diagnosis and therapy or nonspecific and papillitis. Late stages of the disease include narrowing of the retinal vessels, Diagnosis of onchocerciasis is done by the micro- optic nerve atrophy, and the development of focal or filariae or adult worms from skin or subcutaneous diffuse atrophic changes in the retinal pigment epi- nodules obtained by biopsy, or by identification of thelium [37,38]. Recently, some cases of bilateral live microfilariae in the aqueous humor. The first DUSN have been described in Brazil by de Souza choice to treat this condition is the macrofilaricidal et al [39]. agent , which is given as a single oral dose Diffuse unilateral subacute neuroretinitis is caused of 150 mmg/kg. Annual ivermectin therapy seems to by a solitary nematode of two different sizes migrat- improve intraocular inflammation [25–27]. Although ing in the subretinal space. The smaller nematode, used routinely, control strategies tend to have measuring 400 to 700 mm in length, seems to be limited success. endemic to the southeastern United States, the Carib- bean islands, and Brazil. The larger nematode, meas- uring 1500 to 2000 mm in length, has been described Diffuse unilateral subacute neuroretinitis in the northern Midwestern United States [40]. The identity of the two worms is unknown. Ancylostoma Diffuse unilateral subacute neuroretinitis (DUSN) caninum and T canis have been suggested to repres- was first described by Gass et al in 1978 [4,28]. It ent the smaller nematode [30,31], but the clinical usually affects healthy patients and can be divided picture and the low rate of serologic evidence of into two stages: the early stage, which is character- infection with Tcanisseems to make Toxocara ized by visual loss, vitreitis, papillitis, and clusters of species an unlikely cause of DUSN [4]. Some multiple evanescent, gray-white outer retinal lesions; patients with DUSN have cutaneous larval migrans, and the late stage, characterized by optic atrophy, before or concomitant with the answer of ocular retinal artery narrowing, diffuse pigment epithelial symptoms, which has led some authors to suggest A degeneration, and an abnormal electroretinogram caninum. procyonis, a nematode found [29]. DUSN is caused by two as of yet unidentified in the intestinal tract of a raccoon, has been sug- species of nematode, both of which can cause pro- gested to be the larger nematode. Tropical varieties of gressive ocular damage [30–33]. T canis and A caninum have been suggested to cause 354 N.A. Sabrosa, M. Zajdenweber / Ophthalmol Clin N Am 15 (2002) 351–356

DUSN in Brazil based on recent morphologic inves- to various organs, such as the skin, , and eye. tigations performed by de Souza EC et al (perso- As mentioned previously, this infestation is prevalent nal communication, 2001). in parts of the developing world where poor hygiene is common, such as Central and South America, Laboratory investigations and therapy India, Southeast Asia, China, and certain parts of Africa [45]. Patients with DUSN usually have a negative systemic evaluation. Atypical presentations should Ocular features, diagnosis, and therapy suggest other diagnosis, however, and laboratory tests should be examined as indications. Electroretinogra- Several sites in the eye can be affected, including phy has value, because most patients with DUSN the subretinal space, the vitreous, the subconjunctival have an abnormal electroretinogram, even if tested space, the anterior chamber, and the . It seems early in the course of the disease. Electroretinogram that larvae use the posterior ciliary arteries to gain is rarely extinguished completely, which can help access to the subretinal space [46]. Diagnosis is differentiate DUSN from the tapetoretinal degenera- typically made by observing Cysticercus within the tions [3,41]. Recently, it has been noticed that Gold- eye. The larvae can be seen in the vitreous once they man perimetry may be useful to evaluate remaining cross the retina, leaving a retinochoroidal lesion or visual field before and after treatment of the disease scar at the point of exit. ELISA for to (de Souza EC, personal communication, 2001). endemic types of may be helpful, and in Therapy is limited in patients with DUSN. If the some cases are evidence. Slit lamp worm is visualized, laser treatment of the nematode examination or B-scan ultrasonography may show can be highly effective and may improve visual acuity movement of living in some cases. Medical and inflammatory ocular signs, according to Gass treatment of cysticercosis may cause serious visual [35,42]. The worm can be induced to migrate away loss, because the degeneration of the can pro- from the macula before treatment by directing a bright duce severe inflammation [47]. Surgical removal of light on it. The worm may also be surgically removed intraocular cysts is usually recommended [48]. for identification purposes [31]. Chemotherapy with Vision may be irreversibly affected when the macula anthelmintic drugs, such as thiabendazole, may be the is involved. only treatment available when a worm cannot be visualized, but success is often difficult to document. Treatment with corticosteroids has shown tran- Summary sient suppression of the inflammation without alter- ing the final outcome of the disease [34,42]. Patients Nematode infections of the eye are common in with retinal complications caused by the inflam- different parts of the world, but some are usually mation may benefit from surgical intervention in encountered only in developing nations, such as some cases. onchocerciasis and cysticercosis. Ocular toxocariasis is a well-known cause of unilateral ocular disease affecting mainly children and young adults, and is Cysticercosis usually caused by Tcanis. Prevention of ocular toxocariasis is based on such measures as appropriate Cysticercosis is a common cause of ocular health care for dogs and cats, including regular inflammation in some developing countries. Cysti- anthelmintic treatments, preventing contamination cercus cellulosae is the larvae of , and of the environment with feces, and promoting is the most common tapeworm to invade the eye. responsible pet ownership [1,49–51]. Onchocerciasis The ingestion of T solium eggs, which occurs when is caused by infection with the filarial parasite undercooked infected with cysticerci is O volvulus, and occurs in endemic areas along rivers ingested, causes cysticercosis [43]. The soil and the and streams. In hyperendemic areas almost every environment are contaminated when is person is infected and about half of the population poor. Usually the eggs develop into larva only when is eventually blinded by onchocerciasis. Because of they are ingested by an intermediate , such as this, elimination of host-vector contact is very impor- , but humans can play this role when eggs are tant. DUSN is caused by a motile nematode and is ingested in contaminated food and water [44]. Once found in the Southeastern and Midwestern United larvae penetrate the intestinal wall and gain access to States and in many parts of the world. 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