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A 3-year-old boy with a history of eating dirt was determined to have hepatomegaly on routine physical examination by his pediatrician. On questioning, his mother reported that his abdomen had been distended for at least 6 months; however, except for occasional coughing and wheezing, the child had been well. Laboratory investigation revealed a normal hemoglobin concentration, but a high WBC count (21,400 WBC/mm(3)), with 42% eosinophils. Parasite eggs were not observed on examination of feces. Enzyme-linked immunosorbent assay titer for Toxocara antibody was 1:512, and the child was determined to have visceral larva migrans. Serotesting of the patient's 2 siblings, 4 and 6 years old, revealed high antibody titers; however, except for slightly high eosinophil counts, the results of physical examinations were not remarkable. Ophthalmologic examinations on the 3 children did not reveal evidence of ocular invasion by Toxocara larvae. The patient's family had obtained a pup approximately 6 months before the patient developed symptoms, and all of the children had played with the pup in their backyard. The parents were instructed by the physician to forbid their children to play unattended in the backyard, because the soil was possibly contaminated with dog feces that contained Toxocara eggs. The patient recovered without specific treatment. The patient's mother called her veterinarian and asked the following questions:

Q: What is larva migrans?

A: Larva migrantes are human diseases caused by migration of certain parasite larvae in the organs and tissues.¹ Toxocara sp, the common roundworms of dogs and cats, are by far the most common; however, other species of nematodes, such as Baylisascaris sp, hookworms, Strongyloides spp, gnathostomes, and others found in various host mammals are capable of causing disease in human beings.

Q: What are Toxocara spp?

A: Toxocara spp (family Ascaridae) are large, heavy-bodied nematodes, the adult stages of which reside in the small intestine of their final host. Two species infect dogs and cats: Toxocara canis in dogs and other canids²; Toxocara cati in cats and other felids.³

Adult Toxocara have a life span averaging 4 months. Individual female T canis can produce 200,000 eggs/day, and because intestinal worm burdens range from one to several hundred worms, infected animals can contaminate the environment daily with millions of eggs.

Q: How are these parasites transmitted in dogs and cats?

A: Toxocara sp are well adapted for transmission and survival.^2-5 Dogs can become infected with T canis by ingestion of infective eggs, ingestion of larvae in tissues of paratenic hosts, (mice, birds, pigs, earthworms, and others), transplacental migration of larvae from a pregnant bitch to her developing pups, transmammary passage of larvae in milk from a lactating bitch to nursing pups, and ingestion of late-stage larvae or immature adults in the vomitus or feces of infected pups.⁶ When mature dogs ingest Toxocara eggs, most larvae do not undergo further development and translocation to reach the dog's intestine; rather, they are distributed to somatic tissues--principally the lungs, liver, kidneys, and muscles. In the pregnant bitch, tissue-stage larvae become mobilized during late gestation and migrate transplacentally to infect the pups. The transplacental route of infection is so efficient that, unless heroic measures have been taken to eliminate larvae from bitches, nearly all pups are born with Toxocara larvae in migration, which by the fourth postpartum week have matured in the pups' intestines and are producing eggs. The life cycle of T cati in cats is similar to that of T canis in dogs, except that there is no placental transfer of larvae.^3,7

Q: How do human beings become infected with Toxocara sp?

A: People become infected when they ingest infective Toxocara eggs in the soil or on contaminated hands or fomites.⁵ Because Toxocara eggs require a prolonged extrinsic incubation period (2 weeks or more) before larvae developing within become infective, direct contact with infected dogs or cats plays a secondary role in transmission. An important exception may be the nursing bitch and her pups. Intense egg excretion by the confined pups results in persistent contamination of the entire litter area (including the pups' coats) with infective eggs, and persons handling pups at this time are at risk of becoming infected unless they wash their hands thoroughly.

Q: How does Toxocara induce disease in human beings, and what are the clinical manifestations of toxocara larva migrans?

A: Ingested eggs hatch in the small intestine, and the larvae (350 to 450 µm x 16 to 20 µm) penetrate the mucosa, migrate to the liver via the portal circulation, follow vascular channels to the lungs, and then enter the systemic circulation and somatic tissues. Larvae migrate extensively through the body and have been found in virtually every tissue and organ system including liver, lungs, heart, and brain. The clinical and pathologic manifestations result from the mechanical damage caused by the migrating larvae and by the often severe inflammatory response stimulated by their presence.^4,5 Affected tissues contain multiple eosinophilic abscesses and allergic-type eosinophilic granulomas.

Infection by few larvae, the most common event, is usually asymptomatic. Two distinct forms of disease produced by Toxocara are classic visceral larva migrans (VLM) and ocular larva migrans (OLM).^5,8 Typically, the VLM syndrome, caused by migration of larvae through somatic tissues, is characterized by fever, leukocytosis, persistent eosinophilia, hypergammaglobulinemia, and hepatomegaly. Pulmonary involvement, with symptoms including bronchiolitis, asthma, or pneumonitis, is common. The few human fatalities that have been caused by Toxocara have resulted from extensive involvement of the myocardium or CNS or from an exaggerated immunologic response.

Invasion of the eye by Toxocara larvae is not uncommon, although the frequency of ocular invasion as a proportion of total infections is unknown. Ocular larva migrans differs in several important respects from VLM. Ocular disease usually is seen in the absence of other signs or symptoms of VLM, and history of pica (compulsion to eat nonfood items) is less common. Although many cases of OLM are reported in adults, the mean age at diagnosis is 7 to 8 years old, compared with 1 to 4 years old for VLM.

Q: How common is Toxocara infection in human beings?

A: Although a serologic survey of the US population measured toxocara seroprevalence at 2.8%, most of these infections were presumably asymptomatic.⁵ Since toxocaral larva migrans is not a reportable disease, reliable incidence data are not available. The nonspecific clinical signs and symptoms probably result in underdiagnosis. One indication that toxocariasis is a common presumptive clinical diagnosis in the United States is the large number of serum specimens submitted to the National Centers for Disease Control for serodiagnostic confirmation of toxocariasis. Since 1978, that number has varied each year between 2,000 and 3,500; one quarter to one third of the specimens are seropositive. Questioning of physicians attending 119 patients who were seropositive indicated that 72% had OLM, 20% had VLM, and the remainder were asymptomatic.^a Ninety-five percent of patients with OLM had faulty vision, including 20% who were blind in one or both eyes. Fifteen had leukocoria and one eye was enucleated.

Q: Who is most likely to become infected?

A: Serologic surveys indicate that infection rates varied greatly with age, race, and socioeconomic status.^5,9 Seroprevalence is highest in children less than 12 years old, but declines markedly with advancing age. Seroprevalence is higher for blacks than whites of all ages, is higher in rural areas than in urban areas, and is highest among people of the lowest socioeconomic classes.

A history of eating dirt is a finding in the majority of children with VLM.^5,8 In the United States, children with toxocariasis are much more likely to have kept a dog in the house or yard within 1 year of onset of symptoms, when compared with sex- and age-matched controls.^10,11 However, in Britain, about 50% of patients had never owned a dog or cat and had only slight and transient contact with them.¹² Most of these patients were presumably exposed to Toxocara eggs in contaminated soil in parks and public places.

Q: Are veterinarians at high risk of acquiring toxocariasis?

A: Recent studies of groups commonly exposed to pets found that kennel workers, veterinarians, and veterinary assistants do not have greater serologic evidence of toxocariasis than do matched nonexposed control groups. This suggests that observance of routine hygiene by trained persons is adequate to avoid infection.^12-14

Q: How can transmission of Toxocara infections from pets to children be prevented?

A: There are 3 important considerations:

• Prevent fouling of yards and public places, especially childrens' playgrounds, with dog or cat feces.
  
  
• Educate pet owners about the potential human health hazards of roundworms in pets and how to avoid them. Pet owners should be informed of the modes of transmission and of the special risks associated with pups and nursing bitches.
  
  
• 7 Eliminate roundworms from dogs and cats by appropriate treatments.^4,5

Q: What drugs are most efficacious for eliminating intestinal roundworms from dogs and cats?

A: Many safe and effective anthelmintic drugs are available to treat ascarid infections in dogs and cats.^4,15,16 Piperazine compounds are effective, practically nontoxic, inexpensive, and continue to be the most common ascaricidal drugs used by practicing veterinarians.¹⁷ However, other compounds have been introduced that have similar efficacy, tolerance, and, in some cases, a broader spectrum of activity against other intestinal helminths of clinical important in dogs and cats (Table 1).

Factors such as spectrum of efficacy, safety in young animals, and cost should be considered in choosing the anthelmintic appropriate for specific needs. For maximal effectiveness in eliminating intestinal worms and preventing excretion of eggs, the correct therapeutic dose of the selected drug should be given to the pet at strategic intervals.

Q: When should treatments be administered?

A: Attention should be focused on the new litter, recently acquired pup or kitten, and the nursing bitch, because they will almost always pass large numbers of eggs. Pups and kittens should be treated at 2, 5, and 11 weeks old. Repeated treatments are necessary because of continued acquisition of infective larvae from milk throughout lactation and from ingestion of infective eggs in the environment. Lactating bitches and queens should be treated at the same time as their offspring. Two treatments, 10 to 14 days apart, should be adequate for newly acquired weaned pups and kittens. Older dogs and cats can be treated as indicated by fecal examination or prophylactically once or twice a year.

To ensure appropriate timing of treatments for pups whelped at private homes, the owners should be provided with appropriate drugs to administer, as instructed by the veterinarian. Owners should be advised to promptly dispose of expelled worms by burning or flushing down a toilet.

Q: Shouldn't anthelmintic drugs be given only on the basis of results of a fecal examination?

A: The high frequency of prenatal Toxocara infections in pups, the disease-inducing potential of migrating larvae, and the public health dangers posed by patent infections warrant prophylactic treatments according to the schedule recommended. To prevent egg excretion and to avoid morbidity and mortality, pups and kittens should be treated before prenatally and lactogenically acquired infections become patent. Moreover, since most new animals are not seen by veterinarians until they are 6 to 8 weeks old, waiting until an office visit to perform a fecal examination means that most pups and kittens will go untreated for 1 month or more after they have begun passing eggs.

Q: Can an adult female dog or cat be treated to remove tissue-stage Toxocara larvae, and thereby prevent transmission to her future offspring?

A: An easy inexpensive way for ridding animals of somatic ascarid larvae is not yet available. Successful establishment of ascarid-free dog colonies requires isolation and repeated treatments of bitches for several generations to prevent reinfection and gradually reduce and eliminate the larvae in the tissues.¹⁸ Although arrested larvae are more resistant than adults to anthelmintics, strategic advantage can be taken by continuously administering anthelmintics to pregnant bitches during the periods when the larvae are reactivated. Daily administration of fenbendazole (50 mg/kg of body weight day) to bitches from the 40th day of gestation to the 14th day after parturition diminishes the numbers of Toxocara (and Ancylostoma caninum) that become established in their pups by 98% to 100%.^19,20 If treatment of bitches is discontinued at parturition, the reduction in the pups' worm burdens is less.²⁰ Higher doses of fenbendazole or albendazole (150 mg/kg/day) given to adult dogs for only 3 days reduced somatic worm burdens recoverable from the tissues by 90%.²¹ Thus, the administration of anthelmintics to the bitch before pregnancy might prevent prenatal transmission to future litters, unless the bitch acquires a new infection during pregnancy or early lactation.

The problem can be solved more simply in cats, because direct perinatal transmission from nursing queens to kittens occurs only via the queen's milk. Eliminating patent intestinal infections from pregnant queens, and hand rearing kittens on prepared formula should result in ascarid-free kittens in one generation. The use of chemotherapy directed at tissue-stage larvae in cats has not been reported, but might be presumed to have the same limitations as described for dogs.

Q: Is it possible to clean up soil and other environments once they have been contaminated with Toxocara eggs?

A: Once deposited in the environment, Toxocara eggs may survive for months or years depending upon soil type and climactic conditions.²² Optimal conditions for accumulation, concentration, and survival of eggs exist in moist soil adjacent to kennels or around doghouses where dogs have been chained.^4,5 No chemical is known to be effective for killing the eggs in soil, although eggs rapidly disintegrate when exposed to full sunlight or dessication. Toxocara eggs in soil can be put out of reach of children by turning over the top soil to bury the eggs. A flame-gun can be used to destroy nematode eggs on concrete floors.²³ Alternatively, after surfaces are physically clean, they may be mopped or sprayed with 1% sodium hypochlorite to strip off the outer protein coat of the eggs so they won't stick to surfaces and can be rinsed away.²⁴ Children's sandboxes can be decontaminated by replacing the sand or by steam sterilization.²⁵

Discussion

The frequency with which Toxocara sp infect human beings is a function of the prevalence of infection in dogs and cats, the degree and types of contact between people and these pets, and the likelihood that people ingest soil or other objects likely to be contaminated with dog or cat feces. Studies in North America suggest that the potential for zoonotic infection is high. The efficiency of prenatal and lactogenic transmission of Toxocara infections results in high rates of infection in both pups and kittens,^4,5 and the proportion of American households owning dogs (42.5%) and cats (28.4%) is probably higher than ever before.²⁶ The fact that households with children are more likely to have pets than those without also is of epidemiologic importance. Occupants of households without pets may be exposed to Toxocara eggs in parks and public places; surveys have determined that 1 to 30% of soil samples are contaminated with Toxocara eggs.^4,5 All children, because of their normal exploration of the environment and less fastidious hygiene, are prone to ingest small amounts of soil if given the opportunity. Children with pica, a habit found in approximately 10 to 30% of children between 1 and 6 years old,(270 almost inevitably become infected if exposed to a contaminated environment. Thus, it is easy to understand why toxocariasis is a common infection (as determined from serologic surveys), particularly among poor children in rural areas.

Most cases of human toxocariasis are preventable by simple measures such as careful personal hygiene, eliminating intestinal parasites from one's pets, and, for parents, being alert to the necessity for not allowing children to play in potentially contaminated environments. Unfortunately, few people are aware of the potential health hazards associated with pets and thus are unmotivated to inquire about or to take the necessary precautions.^4,28 Surveys of the families of patients with larva migrans and of pet owners in general reveal a remarkable ignorance of potential zoonoses (except for rabies).^10,11

If dog and cat owners are to manage their pets so as to avoid infections in their families and not expose other persons to unnecessary risks, they must be informed about certain zoonoses.^4,5,28 Veterinarians could be effective in reversing this trend by systematically providing pet owners with sound advice about reducing zoonotic risks. They are uniquely suited for this role because of their special knowledge and their rapport with pet-owning clients and because a very high proportion of pet owners avail themselves of veterinary services.^10,11,26 By playing an active public health educational role, the veterinarian is demonstrating not only his/her concern for the clients' pet but also for the family and the entire community.

Footnote

(a) Cantor FL, Schantz PM, Pollard R, et al. Surveillance of human toxocariasis. Abstr Annu Meet Am Soc Trop Med Hyg 1984.

References

1. Beaver PC. The nature of visceral larva migrans. J Parasitol 1969; 55:3-12.

2. Sprent JFA. Observations on the development of Toxocara canis Werner, 1782) in the dog. Parasitology 1958; 48:184-209.

3. Sprent JFA. The life history and development of Toxocara cati (Schrank, 1788) in the domestic cat. Parasitology 1957; 46:54-77.

4. Schantz PM, Glickman LT. Roundworms in dogs and cats: veterinary and public health considerations Comp Contin Vet Educ 1981; 3:773-784.

5. Glickman LT, Schantz PM. Epidemiology and pathogenesis of zoonotic toxocariasis. Epidemiol Rev 1981; 3:230-250.

6. Sprent JFA. Research note: post-parturient infection of the bitch with Toxocara canis. J Parasitol 1961; 47:284.

7. Swerczek TW, Nielson SW, Helmboldt CF. Transmammary passage of Toxocara cati in visceral organs of experimental animals. Acta Vet Hung 1971; 21:405-412.

8. Zinkham WH. Visceral larva migrans. Am J Dis Child 1978; 132:627-633.

9. Hermann N, Glickman LT, Schantz PM, et al. Seroprevalence of zoonotic toxocariasis in the United States: 1971-1973. Am J Epidemiol 1985; 122:890-896.

10. Schantz PM, Weis PE, Pollard ZF, et al. Risk factors for toxocaral ocular larva migrans: a case-control study Am J Public Health 1981; 70:1269-1272.

11. Schantz PM, Meyer D, Glickman LT. Clinical, serologic and epidemiologic characteristics of ocular toxocariasis. Am J Trop Med Hyg 1979; 28:24-28.

12. Woodruff AW, De Savigny D, Jacobs DE. Study of toxocaral infection in dog breeders. Br Med J 1978; 2:1747-1748.

13. Glickman LT, Cypess RH. Toxocara infection in animal hospital employees. Am J Public Health 1977; 67:1193-1195.

14. Jacobs DE, Woodruff AW Shah Al, et al. Toxocara infections and kennel workers. Br Med J 1977; 133:51.

15. Roudebush P. An updated guide to chemotherapy of small animal intestinal parasites. Canine Pract 1985; 12:7-20.

16. Schillhorn van Veen TW, Bukowski IA. Intestinal helminths: a perennial problem in pets. Vet Med (Suppl) 1986; 4-9.

17. Kornblatt AN, Schantz PM. Veterinary and public health considerations in canine roundworm control: a survey of practicing veterinarians. J Am Vet Med Assoc 1980; 177:1212-1215.

18. Griesemer R, Gibson JP. The establishment of an ascarid-free beagle dog colony. J Am Vet Med Assoc 1963; 143:965-967.

19. Burke TM, Robertson EL. Fenbendazole treatment of pregnant bitches to reduce prenatal and lactogenic infections of Toxocara canis and Ancylostoma caninum in pups. J Am Vet Med Assoc 1983; 183:987-990.

20. Duwel D, Strasser H. Versuche zur Geburt helminthenfreier Hundewelpen durch Fenbendazol-Behandlung. DTW 1978; 85:198-272.

21. Lloyd S, Soulsby EJL. Prenatal and transmammary infections of Toxocara canis in dogs: effect of benzimidazolecarbamate anthelmintics on various developmental stages of the parasite. J Small Anim Pract 1983; 24:763-768.

22. Owen WB. Factors that influence the development of the ova of an ascarid roundworm Toxocara canis (Werner 1782) Stiles 1908, under field conditions. Univ Minn Agric Exp Stn Tech Bull 1930; 71:3-25.

23. Pegg EJ. A new approach to the control of Toxocara canis and other parasitic ova on concrete-floored kennel runs. Br Vet J 1977; 133:427-431.

24. Georgi JR. Parasitism of dogs and cats. Parasitology for veterinarians. 4th ed. Philadelphia: WB Saunders Co, 1985; 145-159.

25. Van Knapen F, Franchimont JH, Otter GM, et al. Steam sterilization of sandpits infected with toxocara eggs. Br Med J 1979; 1:1320-1321.

26. Wise JK, Kushman JE. Pet ownership by life group. J Am Vet Med Assoc 1984; 185:687-690.

27. Bicknell J. Pica: a childhood symptom. London: Butterworth & Co Ltd, 1975; 4-25.

28. Stehr-Green JK, Schantz PM. The impact of zoonotic diseases transmitted by pets on human health and the economy Vet Clin North Am [Small Anim Pract] 1987; 17:1-15.

Addendum (1994)

The Centers for Disease Control and Prevention (CDC) has printed a new pamphlet, "How to Prevent Transmission of Intestinal Roundworms from Pets to People: Recommendations for Veterinarians." Written by the American Association of Veterinary Parasitologists, in collaboration with the CDC, the pamphlet is endorsed by the National Association of State Public Health Veterinarians and the Conference of Public Health Veterinarians.

The guidelines recommend strategically timed preventive anthelmintic treatments for pups and kittens. Details are provided on advising pet owners how to avoid the zoonotic disease risks.

Copies (specify number needed) may be ordered from Dr. Peter M. Schantz, Division of Parasitic Diseases, NCID(F22), Centers for Disease Control and Prevention, 4770 Buford Hwy, Atlanta GA 30341-3724; phone (404)488-7767; fax (404)488-7761.