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Toxocara Canis infestation with encephalitis

NADIA Z. MIKHAEL, VITAL J. A. MONTPETIT, MANUEL ORIZAGA, HARRY C. ROWSELL, MICHAEL T. RICHARD

SUMMARY: The syndrome "visceral not verified. We believe the present re­ INTRODUCTION larva migrans" produced by migration port is the first verified case of visceral Toxocara canis, the common of nematode larvae (commonly Toxo­ larva migrans in Canada and the fifth roundworm of the dog, is harmful to cara species) in the extraintestinal case of human cerebral involvement by man and is a public health problem. tissues in unusual hosts, including man Toxocara in the English literature. It is There is a large reservoir of Toxo- (particularly children of dirt eating age), hoped that this report will emphasize caral infestation in dogs in many with the production of reactive granu­ the need for further research into the role lomatous lesions, was first described in of host versus parasite and will under­ countries, including Canada. The 1952. About 200 cases have been re­ line the potential danger, albeit remote, incidence of Toxocariasis in Canada ported since. Well documented cases of household pets to children. Indeed, is unknown but is probably com­ are rare due to the difficulty in histo­ prevention is the only line of attack, as moner than this single case report logical verification. Three cases have there is no effective drug against the mi­ indicates. The prime difficulty in this been reported in Canada but these were grating larvae of Toxocara. infestation is that it gives rise to larvae which migrate in the tissues but do not develop beyond the second stage in man. The larvae are RESUME: Le syndrome "visceral larva rapporte ci-dessous est le premier cas small, and because as few as 20 may migrans", cause par la migration de connu au Canada dont la verification cause significant illness, it is certain larves nematodes (le plus frequemment a prouve la presence de larva migrans, that in most cases it will be difficult de I'espece toxocare) dans les tissus et le cinquieme cas d'atteinte cerebrate to diagnose the infestation by re­ extra-intestinaux et qui se developpe, par Toxocara decrit dans la litterature covering the larvae. A prolonged accompagne de lesions granulomateuses anglaise. Nous esperons que ce rapport search through many serial sections reactives, chez des holes inhabituels, servira a mettre V accent sur le besoin is usually necessary to locate a larva y compris I'homme (particulierement les de recherche supplementaire dans le and even then, only a transverse enfants a I'dge oil ils mangent sale- domaine des relations holes-parasites, ment) fut decrit pour la premiere fois et a souligner le danger potentiel, quoi- section at the level of midgut is en 1952. Bien que deux cents cas aient que vague, que represente la cohabita­ conclusive evidence. Larvae were ete denombres depuis, la verification en tion enfants-animaux domestiques. La identified in our case after examin­ histologic etant difficile, les rapports presentation reste done notre seule res- ing 300 sections. It is the object of precis demeurent rares. Au Canada, on source, etant donne qu'il n'existe aucun this paper to report a fatal case of rapporta trois cas, mais aucun de ceux medicament efficace contre les larves Toxocariasis. This is the first known ci ne fut verifie. Nous pensons que celui migrantes de la Toxocara. verified case of visceral larva migrans in man in Canada and the fifth case of human cerebral involve­ ment by Toxocara in the English literature.

CASE REPORT An 18 month old white male was ad­ mitted to hospital with fever of unknown origin and nasal catarrh of one week's duration. The child was the first born after an uneventful pregnancy and de­ From the Department of Pathology, University livery. During infancy he suffered only of Ottawa, and the Departments of Laboratory occasional colds and had no major ill­ Medicine and Neurosurgery of Ottawa General nesses. He had been found eating dirt Hospital. on numerous occasions in the yard. The Reprint address: N. Z. Mikhael, M.B., B.Ch., family had no household pets. Department of Laboratory Medicine, Ottawa General Hospital, Ottawa KIN 5C8 Ontario, On his first admission the child was Canada. pale, with a temperature of 101°F and a

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slightly enlarged spleen. His hemoglobin the liver and heart and an occasional tained an oblique section through the was 7.2 gm%, WBC was 32,000/mm3 focal hemorrhagic area 0.4-0.5 cm in intestinal region of a Toxocara larva. with an eosinophilia of 64%. X-ray of the diameter in the lungs, pancreas and The valves were normal. The chest showed streaky, abnormal shadow­ spleen. Microscopic examination of epicardium was edematous and con­ ing in the right upper and both lower these lesions revealed granulomata in lobes. A few days after admission, tained scattered foci of neutrophils, rhonchi were heard in the chest and his various stages of evolution. Typical eosinophils and mononuclear cells. leukocyte count went up to 45,000/mm3 Toxocara canis larvae were iden­ Similar changes were also seen in the with no change in the differential. He tified in the liver, heart and brain. myocardial septae. was treated with Ampicillin and ferrous The lungs revealed considerable In the liver, the granulomata were sulphate and showed some improve­ atelectasis and extensive pulmonary numerous and scattered in an irregu­ ment, but his eosinophil count was un­ edema with patchy broncho­ lar fashion. They showed central, changed. The clinical impression at the pneumonia. Scattered throughout time of discharge was that of iron de­ complete, destruction of liver cells ficiency anemia, and possible visceral many sections were granulomata and collapse of reticulum frame­ larva migrans. consisting of a central area of nec­ work, often with "fibrinoid" altera­ rosis surrounded by palisaded He was re-admitted 3 weeks later in a tion of individual fibers. Around the semicomatose state with a 10 day history epithelioid cells and a dense infiltrate center there was the usual dense of shaking spells and ataxia. He re­ of eosinophils, neutrophils, lympho­ exudate of eosinophils, histiocytes, peatedly went into status epilepticus cytes and plasma cells. Some of these rare plasrria cells and occasional giant and was transferred to the Ottawa granulomata contained multi­ cells. Older granulomata with many General Hospital. On arrival, he was nucleated giant cells and were sur­ giant cells surrounded by a layer of comatose, but responded to some stimuli rounded by a concentric layer of col­ collagen fibers were also seen. Many and was able to move all four limbs. lagen fibers. These represented le­ early lesions displayed portions of There was no neck rigidity. His pupils sions of longer duration. were small, equal and reactive to light. second stage infective larvae of Pulse rate was between 120-140 beats/ The heart showed rounded or Toxocara canis (Fig. 1 & 2). The di­ minute. Blood pressure 120/70 and elongated granulomata with darkly agnosis was made on the basis of the temperature 101°F. Examination of the eosinophilic centers containing large characteristic structures of the trans­ heart and chest revealed no abnormali­ amounts of cellular debris sur­ verse section of the larva at the mid­ ties. The liver was palpable 2 cms below rounded by mononuclear cells of gut level, namely: diameter 18-20 the right costal margin; the spleen was epithelioid type together with multi­ micra, prominent single lateral alae, just palpable. The reflexes were physio­ single intestinal cell, and large, well logical. Laboratory data were as follows: nucleated giant cells. Older Hemoglobin 10.4, hematocrit 36%, granulomata as described in the lung defined posterior excretory columns WBC 9,100/mm3, 42% Neutrophils, 40% were also seen. One early lesion con­ occupying a greater proportion of lymphocytes, 4% monocytes, 10% baso­ phils and 4% eosinophils. The platelet count was normal. Urine analysis was normal. CSF sugar was 88 mg% and pro­ tein 320 mg%. The electroencephalo­ gram was abnormal with focal abnor­ malities in the left hemisphere behind the Sylvian fissure and in the right fronto-temporal area. A repeat record showed similar changes in the left pos­ terior frontal region. Echoencephalo- gram showed no shift. Burr hole explora­ tion and left carotid angiography were normal. Liver biopsy showed two granu- lomata of uncertain etiology. The con­ vulsions were only temporarily controlled by anti-epileptic agents. His general con­ dition remained poor and he died 3 days after his second admission and 7 weeks following his first admission.

PATHOLOGICAL FINDINGS Most of the organs revealed mild organomegaly; the liver weighed 440 gms, the spleen 60 gms, the heart 60 gms and the pancreas 30 gms. There Figure 1. Sections of Toxocara canis larvae at the level of midgut with necrotic debris and were multiple, firm, grey-white inflammatory cells in a granuloma of the liver. Note the prominent single lateral alae, nodules up to 0.3 cm in diameter in single intestinal cell and large well defined posterior excretory columns. HPS x 750.

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Toxocara canis, the common roundworm of the dog, is harmful to man and is a public health problem. Man may act as host of these para­ sites. The ingestion of eggs may re­ sult in the migration of Toxocara lar­ vae through the somatic tissues, and subsequent encystment and granu­ lomatous lesions in the various organs of the body. The syndrome was first denned by Beaver et al (1952). Visceral larva migrans is usually due to the most commonly occurring ascarid species, Toxocara canis or Toxocara cati, the roundworms of the dog and cat re­ spectively. Usually it is a relatively benign disease characterized by sus­ tained eosinophilia of 30% or more, hepatomegaly, fever, anemia and pneumonitis. Although the syndrome occurs more frequently in children, adults appear (Snyder, 1961) to be Figure 2. An oblique section through the densely nucleated intestinal end of the susceptible, but are less commonly nematode larva in a sinusoid of the liver. infested because of better personal HPS x 750. hygiene (Dent et al, 1956). the body cavity than the intestine mission of disease. The chance of Since the syndrome was first de­ (Fig. 1). potential contact is increased be­ scribed about 200 cases have been The pancreas and spleen showed cause many pet owners allow their reported (Woodruff, 1970), but well multiple granulomata similar to those pets to defecate in public parks and documented cases are rare. In seen in the liver. other areas frequented by children. Canada, two cases were reported by Throughout the cerebral hemis­ pheres, cerebellum and brain stem, there were multiple, small, sharply demarcated regions of granulomat­ ous inflammation involving both grey and white matter. These appeared to be more recent than those in the vis­ ceral organs, being composed almost entirely of epithelioid cells. In the center of most of these, parts of the coiled nematode, cut in various planes, were observed (Figs. 3, 4, 5). DISCUSSION During the past decade, the recog­ nition of Zoonoses, "those diseases and infections which are naturally transmitted between vertebrate ani­ mals and man", as defined by the World Health Organization, has been one of the advances in Medicine. The dog "man's best friend" is said to have been domesticated about 60,000 years ago and is the one animal which enjoys a closer association with man than any other. The daily social con­ Figure 3. Granulomatous focus in subcortical white matter of cerebral hemisphere tact with this pet, especially with containing three segments of the coiled nematode. children, is conducive to the trans­ HPS x 120.

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-S*B| rarely found (Unrah et al, 1973); (Webster, 1958). The prevalence of "' te.-"- . • ,f*J& intestinal infestation in dogs in differ­ ent countries varies from 2.5% to , •. t^f* s 93% (Table 1), the prevalence being 1 higher among puppies below 6 0 < months of age. The prevalence in Canada varies from 8% to 88% (Table II). The original identification of the parasite, Toxocara canis, is attrib­ uted to Werner in 1782, but it was not until 1958 that the full development of these worms was studied by Sprent. Adult toxocaral worms measure 7.5 to 12.5 cm in length and are of no practical importance in human infec­ tion. The eggs measure 90 x 75 micra and have finely pitted shells. The OV '" ovum takes up to three weeks to de­ velop into an infective larva in a suit­ able environment and remains viable for several months. The larva is a Figure 4. Higher magnification of Fig. 3 showing sections through the isthmus, gastro­ coiled helminth measuring 357 to 445 esophageal junction and midgut level of Toxocara canis larva. micra in length and 18 to 22 micra in HPS x 480. diameter. The structural characteris­ tics of the larva were studied in detail by Nichols (1956). The differentia­ tion between Toxocara canis and cer­ tain other nematodes of similar size is made on the basis of transverse sec­ tions at the midgut level. The diag­ nostic features of Toxocara canis larva are as listed above. The infec­ tive second stage Toxocara canis and cati larvae have almost identical

T % morphology, differing only in their awr -mjr jr% Jk_*TOL - „

LIFE CYCLE The life cycle is comparable to that of Ascaris lumbricoides and has been described in detail by Sprent (1958), and Brain and Allan (1964). In the natural host, the dog, the cycle varies according to the age and sex of the animal. Puppies are invariably in­ fected pre-natally via the placenta. Figure 5. Granuloma in the cerebral white matter containing deeply staining cellular At birth, larvae are found in their debris and a section through the esophageal end of the larva. lungs. These migrate to the trachea, HPS x 300. are swallowed, and, upon reaching McKee in 1957 and one case by and temperate zones. The incidence the upper gastro-intestinal tract ma­ Wong and Laxdal in 1958. None of of infestation in dogs fluctuates with ture into adult worms. By the time these was histologically verified. seasonal variations (Ehrenford, the puppy is about 3 weeks old eggs 1957) but in general Toxocara is more are excreted in enormous numbers. THE PARASITE prevalent in warm climates than in This massive excretion continues Toxocara parasites are widely dis- extreme northern areas. In the until the adult worms die, when the tributed throughout the semitropic Northwest Territories Toxocara is puppy is about 6 months old. Ex-

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TABLE I infection, infective Toxocara ova PREVALENCE OF TOXOCARA CANIS INFESTATION IN VARIOUS COUNTRIES from contaminated soil must gain ac­ cess to the gastro-intestinal tract. i Infested Dogs Countries Investigators Secondly, a search for Toxocara ova Mexico (Mexico City) 93% of 120 dogs Styles 1967 in the stools of an infected human will India (Calcutta) 82.8% of 100 dogs Maplestone & Bhaduri 1940 be fruitless since the larvae never ma­ Sicily 79.5% Gallo & Girolamo 1960 Philippines (Manila) 76.5% of 81 dogs Yutuc 1954 ture in the tissues of a foreign host U.S.A. (New York State) 73% of 64 dogs Styles & Evans 1971 (Zinkham, 1968). England (Cambridge) 70.8% Nuttal & Strickland 1908 Nigeria (Ibadan) 37.5% of 72 dogs Wiseman & Woodruff 1971 CLINICAL PRESENTATION Malta 28.8% of 52 dogs Wiseman & Woodruff 1971 Visceral larva migrans is primarily Tanzania (Dar-es-Salaam) 28% of 50 dogs Wiseman & Woodruff 1971 a disease of small children, and a Australia (Melbourne) 21.8% of 174 dogs Pullar 1946 careful history frequently reveals U.S.A. (Indiana) 21% of 1,465 dogs Ehrenford 1957 pica. The history of pica is more im­ Spain (Madrid) 21% Millan 1959 U.S.A. (Boston) 20% Heiner & Kevy 1956 portant in establishing the source of Iraq (Bagdad) 18.4% Al-Safaar et al 1962 infection than is the ownership of a Wales (Abereswyth) 16.3% Lewis 1927 cat or dog. Chile 15% Neghme et al 1956 The clinical features of this syn­ France (Marseille) 13.5% Solomon 1933 drome depend on the number of lar­ Uganda (Kampala) 12.5% of 116 dogs Wiseman & Woodruff 1971 vae, the frequency of their migration, Kenya (Nairobi) 5.7% of 35 dogs Wiseman & Woodruff 1971 the organ involved and the host's England (London) 2.5% of 161 dogs Woodruff 1970 sensitivity to the Toxocara (Shrand, 1964). Symptoms include fever, ir­ ritability, pallor, anorexia and TABLE II malaise. Hepatomegaly is the most PREVALENCE OF TOXOCARA CANIS IN DOGS IN CANADA common physical finding, varying in Province % Dogs Infested Remarks amount. Splenomegaly is less often Newfoundland* 40% of 200 dogs (35% pups 3 months of age) observed, and when present tends to Nova Scotia* 18% of 385 dogs (13% pups 3 months of age) be minimal. Abnormalities of the New Brunswick* 20% of 204 dogs (18% pups 3 months of age) lungs are common, and physical ex­ Quebec (St. Hyacinthe)* 35% of 211 dogs (14% pups 3 months of age) amination of the chest may reveal (Montreal)** 52.6% of 155 dogs signs compatible with bronchitis, as­ Ontario* 22% of 448 dogs (13% pups 3 months of age) thmatic bronchitis or broncho­ (Ottawa Carleton Dog pneumonia. In many patients the Pound)*** 51% of 51 dogs (all pups 3 months of age) pulmonary changes tend to recur. (Guelph)**** 88% of 1,000 dogs (80% pups below 6 mos. age) Manitoba* 8-10% (Majority pups) Eye symptoms and signs have long Vet clinics been recognized (Ashton, 1960; Saskatchewan* 15% (30% pups 3 months of age) Nichols, 1956; Wilder, 1950) and VSB Laboratory findings resembling retinoblastoma Alberta* 10% U of A. Vivarium and chronic endophthalmitis have * Survey of Veterinary Service Branch Provincial Department of Agriculture 1973 (Personal Communica­ been well documented. tions). A toxocaral larva was found in the ** Choquette L.P.E. and Gelinas L. de G., C. J. of Comp. Med. 14: 33, 1950. myocardium of a patient by Dent et al *** Survey by H. C. Rowsell, Veterinary Service Branch Lab. Ministry of Agriculture & Food, Kempville, Ontario, Canada. (1956), and Friedman and Hervada **** Lautenzlager J. P., Guelph, Ontario (Personal Communications). (1960) reported a case in which the circumstantial evidence for the myocarditis was strong. Woodruff creted eggs can remain viable in the (Sprent, 1958) and wide dissemina­ (1965) suggested that involvement of soil for a year if protected from sun­ tion may occur via the blood stream the myocardium plays a part in the light, freezing and drying (Dorman and lymphatics. Larvae can remain production of the puzzling en­ et al, 1958.) viable in the tissues of man for a year domyocardial fibrosis reported from When the eggs are ingested by or more (Smith et al., 1955), but they Africa in recent years. adult dogs, the larva migrate through eventually die. The granulomatous It is well known that a variety of the body and can live in various tis­ lesions then heal by fibrosis. neurological symptoms can develop sues for long periods. Certain features of the life cycle of in persons harbouring intestinal When the eggs are ingested by Toxocara in its natural and unnatural nematodes (Chalgren et al., 1946). man, they hatch in the small intestine hosts underscore two important as­ The pathogenesis of these manifesta­ and the larvae migrate. Apparently, pects of visceral larva migrans in tions is obscure. It has been sug­ they are particularly active borers man. First, for humans to develop the gested that the symptoms are due to

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the effects of toxins or allergins (Snyder, 1961), and in others the im­ BRAIN, LORD and ALLAN, B. (1964). originating from the parasites provement has coincided with the fall Encephalitis due to Infection with Toxo­ cara Canis; report of a suspected case. (Sprent, 1955 I & II). To date, there in the titre of the fluorescent- Lancet 1, 1355 - 1357. are only four reported cases of antibody test. The dose recom­ BRILL, R., CHURG, J., and BEAVER, P. human cerebral involvement by mended is 3 mg per Kg body weight C. (1953). Allergic Granulomatosis As­ Toxocara canis (Beautyman et al, twice daily for 21 days (Woodruff, sociated with Visceral Larva Migrans: 1951, 1966; Dent et al, 1956; Moore, 1966). case report with autopsy findings of toxo­ 1962; Schochet, 1967). cara infection in a child. American Journal Aur et al (1971), reported rapid of Clinical Pathology, 23, 1208 - 1215. clinical and laboratory improvement CHALGREN, W. S., and BAKER, A. B. DIAGNOSIS in three children with visceral larva (1946). Tropical disease; involvement of Diagnosis is suspected by the clini­ migrans following treatment by nervous system. Archives of Pathology, 41, cal features of the disease in associa­ thiabendazole. Infected animals may 66- 117. be effectively treated by piperazine DENT, J. H., NICHOLS, R. L., BEAVER, tion with persistent eosinophilia. P. C, CARRERA, G. M. and STAG­ Presumptive diagnosis may be made adipate; 200 mg per Kg removes the GERS, R. J. (1956). Visceral Larva Mi­ from the Toxocara skin test (Wood­ majority of worms even in puppies grans with Case Report. American Journal ruff, 1966 and 1970). The skin test (Sprent, 1958) although frequent re­ of Pathology, 32, 777 - 803. does not distinguish between infec­ petition of treatment during the first DORMAN, D. W., VAN OSTRAND, J. R. tions which are recent and active six months of life is necessary. There (1958). A survey of Toxocara Canis and is little doubt that effective deworm- Toxocara Prevalence in the New York and those which are long-standing City Area. New York State Journal of Medi­ and inactive. Active infections may ing of animals will do more than any cine, 58, 2793 - 2795. be detected by a fluorescent-anti­ other single measure to reduce the EHRENFORD, F. A. (1957). Canine ascari- body test (Bisseru et al, 1968; incidence of infestation in man of this asis as a potential source of Visceral Larva Mitchell, 1964) or by hemagglutina­ disease which is difficult to diag­ Migrans. American Journal of Tropical tion techniques (Aljeboori et al, nose, and variable in response to Medicine & Hygiene, 6, 166 - 170. 1970; Kagan, 1958). The degrees treatment (The Lancet, 1972). FRIEDMAN, S. and HERVADA, A. R. (1960). Severe myocarditis with recovery of specificity of these tests are not in a child with Visceral Larva Migrans. entirely clear. 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