Scand J Infect Dis 23: 225-23 I . 199 1

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Families, Parks, Gardens and Toxocariasis

Toxocara canis antibody titres were measured in members of 30 families. 73/140 (52.1 Yo) family members were seropositive for T. canis at a dilution 3 I :50 and 11 (7.8 %) had reciprocal titres g800. Toxocara ova were sought (a) in relation to the 30 families and (b) in the community. No toxocara ova were found in household dust samples. 38 TOof family gardens contained toxocara ova while 6% of soil samples from public parks and open spaces around housing estates were positive. None of the faecal specimens from pet dogs were positive for toxocara ova as compared to 6.2 % of stray dogs. 5.3% of canine faecal samples from the streets contained toxocara ova. In this study household garden soil was a potentially greater source of toxocara infection than soil in public parks and open spaces.

M . R. H. Taylor, MD, Department of Paediatries, National Children’s Hospital, Hareourt Street, Dublin 2, Ireland

INTRODUCTION The larvae of the common roundworm of dogs. Toxocara canis, infect man and can cause 3 clinical entities, visceral toxocariasis. ocular toxocariasis and covert toxocariasis ( I ) . Children aged 1-4 years with a history of pica are particularly at risk for visceral toxocariasis ( 2 ) . Transmission to humans occurs by the ingestion of viable eggs, most probably from contaminated soil, hands or other objects. Direct contact with infected dogs may be less important because of the time required for embryonation of ova to infectivity (3). In the past emphasis has been placed on the importance of public parks as sources of infection with soil-borne toxocara ova (4,5). The present study of a group of families indicates that the domestic garden may be a more important source of toxocara ova.

MATERIALS AND METHODS Family study 149 people from 30 Caucasian families were investigated. One child from each family was attending the National Children’s Hospital because of asthma. The children were from 1.5-1 5 years. All the families lived in built up areas within County Dublin. Toxocara antibody titres were measured in serum samples from family members. If the family owned a dog or cat a faecal sample was obtained from the pet and examined for ova. Soil samples were obtained from each household that possessed a garden or had access to a green space close to the house. These were examined for toxocara ova. Household dust samples were also examined from 27 of the houses of which 14 had a dog and 1 a cat. Community study The community study involved a 3-part survey: ( I ) an analysis of canine faecal samples from streets, grass verges and public parks adjacent to the homes of those in the family study; (2) an analysis of soil samples collected from public parks and public green areas around other housing estates; ( 3 ) an analysis of canine faecal samples from the Dublin Stray Dog’s Home which has a catchment area covering Dublin city and county. 15 -91 5 5 5 2


C. Holland et al.

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Faeces and sera Approximately 5 g of each stool sample was analysed for parasite ova and cysts by the formyl-ether method ( 6 ) .Faeces were also examined for salmonellae, shigellae. campylobacter and enteropathogenic Escherichia coli. Toxocara titres were measured by enzyme linked immunosorbent assay (ELISA) (7) at the Scottish Parasite Diagnostic Laboratory (SPDL) and the Toxocara Reference Laboratory, London. Soil and household dust Soil samples were collected between February and June 1986. Garden soil samples were taken from where the children usually played. Samples of approximately 250 g, were obtained by scraping an area 130 cm2 with a garden trowel to a depth of 2 cm. In the laboratory the samples were thoroughly mixed and broken into smaller particles. Any sticks, stones or other debris were removed. Two 30 g subsamples were stored at 4°C until analysed. The centrifugal flotation method (8) was used to detect Toxocara species ova. No attempt was made to distinguish T. canis ova from T. cati ova. They are regarded as virtually indistinguishable by light microscopy. Dust samples were obtained from vacuum cleaners or as sweepings from floors and carpets and analysed in the same way.


Family study Faeces. Faecal samples were collected from 26/65 adults and 53/84 children. Cysts of Giardia lamblia were found in specimens from 4 subjects, ova of Enterobius vermicularis from 2, and 1 grew E. coli 0125. These samples were all from children. Neither cysts, parasite ova nor bacterial enteropathogens were detected in the remaining samples. Toxocara titres. Serum was obtained from 140/149 family members. 73/140 (52.1 O/o) family members were seropositive for T. canis excretory-secretory antigen at a dilution 2 1 : 50 and 11 (7.8 Yo) had titres 2 800. Five families had no seropositive members (Table I). Soil and household dust. 26 gardens were sampled (3 gardens could not be sampled, 1 family had no garden and no green area nearby). Samples from 10 gardens (38%) contained toxocara ova (see Table I). The majority of the larvae within the embryonated eggs were motile indicating that they were viable infective agents. No significant statistical association was found between the presence of toxocara ova in the household garden and seropositivity (for 3 5 0 titre chi-square=0.003, DF= 1, p=0.96; for 3800 titre chi-square=0.105, DF= 1, g=0.75). No toxocara ova were detected in the household dust samples. Pets. 16 families owned 1-2 dogs and 1 a cat at or immediately before the time of interview. Faeces were not obtained from the cat. Faecal specimens from 10 dogs were examined and no toxocara ova were found. All the pets were wormed from monthly to once a year except for those of 2 families which were never wormed. Faeces could not be obtained from the unwormed dogs but garden soil samples from both these households contained toxocara ova. Apart from one 8-month old puppy all pets were > 2 years old. No significant relationship was found between dog ownership and seropositivity (for 2 50 titre chi-square=0.238, DF= 1, g=0.63, for 2800 titre chi-square=0.58, D F = 1, p=0.45). 11 households had no pet dog and only 2 of these had ova present in garden soil samples, while 8/15 households with a pet dog had ova in their soil samples, but this difference did not reach statistical significance (Fisher exact test, p=O.11). Community study 1. Analysis of canine faecal samples from streets, grass verges and public p a r h adjacent to where the study families live. A total of 150 samples were collected from 23 sites and 5-10 samples were collected from each site. Eight samples (5.3 O/o) from 7 sites contained toxocara ova (Table 11).

Toxocara antibodies and toxocara sources 227

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2. Analysis of soil samples from public parks and around other housing estates. 53 samples were collected from 17 sites and 2-6 (usually 3) were taken from each site. Larger numbers of samples were taken from large sites and smaller numbers from small sites. Three samples (5.6%) collected from 2 sites contained toxocara ova (Table 11). 3. Analysis oycanine faecal samplesfrorn the Stray Dogs Home. Faecal samples from stray dogs unclaimed after 7 days were examined. Samples were obtained from the rectum at post mortem examination. Details of the dogs age, sex and breed were recorded. The details in relation to age and sex are given in Table 111. Toxocara ova were more commonly found in bitches and in those < 1 year of age but in neither case did this reach statistical significance (for sex, Fisher exact test, p=0.77; for age, Fisher exact test, p=0.14). DISCUSSION The seroprevalence among this group of families, if 800 was taken as the lowest titre considered positive, was 7.8%. Examination of 137 sera from these families by the Toxocara Reference Laboratory, London taking 0.3 as the lowest titre considered positive produced a seroprevalence of 6% (8% for those < 15 years old) (1). In the present study if a titre of 2 50 were taken as positive, these families (based on 140 sera) would have a seropositivity rate of Table I. Seroprevalence of toxocariasis in sludy households with corresponding information on the prevalence of Toxocara spp. ova in gardens Seroprevalence

No. of subjects at each antibody level" House no. I

2 3 4 5 6

I 8 9 10 11 12 13 14 15 16 18 19 21 22 23 24 25 28 29 30

Total no. ova (unembryonated) 0 0 1 5 (1) 0 19 (0) 151 (8) 0 0 0 2 (0) 0 3 (0) 3 (0) 0 0 0 0 2 (1) 0 0 6 (1) 2 (0) 0 0 0 1 (0)

Reciprocal titres.



4 4 1 2

1 2

2 1

4 3 3 2 2 2

2 2 1


1 1 1



6 6 2 4 3



4 2 2


2 2 4

I 00-400


5 1 4 6 3 4 2 1 3

2 3



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228 C. Holland et a/.

Scand J Infect Dis 23 (1991)

5 2 Yo. 129 paired sera from these families were examined both in London and in Glasgow. The results using the cut off criteria of 0.3 for London and 800 for Glasgow were: London 8 positive (6.2 Yo), Glasgow 9 (6.9 Yo).At a 1 : 50 dilution, 63 (48.8 Yo) examined in Glasgow gave a positive result. British seroprevalence rates varying from 2.6% in adults (7) to 14.3% in schoolchildren (9) and 15.7% in dog breeders (10) have been reported. An 86% seroprevalence rate has been reported in St. Lucian children (1 1). Not all studies have reported the levels they considered positive and this makes comparisons difficult. Whereas the serum samples submitted to the SPDL were analysed for antibodies to T. canis excretory/secretory antigen as a series of doubling dilutions starting at 1 : 50, at or above which a sample is deemed positive, those submitted to the Toxocara Reference Laboratory, London were analysed at a spot dilution of 1 : 1000. At comparative titres (800 SPDL, 1 000 London) similar results were obtained (6.9% and 6.2 YO antibody positivity respectively). Larvae can be long lived in human hosts, during which time no multiplication occurs, and a few larvae can cause clinically apparent disease if they induce pathology at a critical site. For this reason it is as important to detect antibody at low serum dilutions as at high dilutions as analyses at low serum dilutions are more likely to detect infection with small numbers of larvae. Indeed, ELISA titres as low as 4 have been diagnostic in histologically proven ocular toxocariasis. Various starting dilutions of serum are used in different laboratories, and at the Communicable Diseases Centre, Atlanta, USA an initial serum dilution of 1 : 32 is used. It was, however, felt that naturally occurring A and B blood group antibodies might compromise

Table 11. Prevalence of toxocara ova from various source5 Samples positive for toxocara ova

No. of sites


or gardens

Siteslgardens positive for toxocara ova (Yo)













No. of samples

Sample site Garden soil Soil from parks, housing estates and green areas Canine faecal samples (general environment) Canine faecal samples (Stray Dog’s Home) Household pet dogs Household dust

80 10 27


0 0

Table 111. Analysis of canine faecal sarnplesfrorn the Stray Dog’s Home by age and sex of dog No. of samples

No. (Yo) positive

23 51

3 (13.0) 2 (3.5)

48 32

2 (4.2) 3 (9.3)


5 (6.2)

for Toxocara canis


G I year > 1 year Sex Male Female Total

To.vocara rrnfiboclies and fo.\-ocara sources 229

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S c a d J infect Dis 23 (1991)

the specificity of the SDPL assay at this dilution. hence a starting dilution of 1 : 50 was chosen 9 years ago. At a 1 : 50 dilution 52 O/o of sera were positive. This percentage seropositivity is far higher than the values reported for the United Kingdom, or by the SDPL previously, and indicates that a high level of covert toxocaral infection exists in the families studied. Using a 1 : 50 dilution the seroprevalance rate in Scotland is approximately 2 %. The soil samples from gardens showed a higher prevalence of toxocara ova than those recorded in similar studies (Table IV). However soil samples collected from the gardens of French adults suffering from toxocariasis and a control population revealed T. canis eggs in 7/29 samples (24.1%)from patient’s gardens and in 5/49 samples (10.2%) collected from similar sites of neighbourhood controls (1 3). The only comparable levels are from sandboxes which are known to be common dog defaecation sites (1 2). It is important to remember that the gardens sampled in the present study are not a random selection, but belong to families each with a child attending hospital because of asthma. In the present study no significant association was found between the presence of toxocara ova in the garden and the seropositivity of the household nor between dog ownership and seroprevalence. This may be due t o the small sample size or the likelihood that infection may be acquired from other sources. The prevalence of toxocara ova in public parks is lower than that found in some comparable studies but in keeping with results from Leeds and Brighton (Table IV). Smith et al. (14) emphasise that their results from individual backyards are considerably higher than those from public spaces. They suggest that rainfall may be less likely to wash ova away from a confined space than an open space and so affect egg density. Whatever the reason both that and the present study have found higher positivity rates in domestic gardens than in public open spaces.

Table IV. The prevalence of toxocara ova from (A) parks and recreational areas and (B) gardens Prevalence Locality A Kansas, USA, Baton Rouge, Louisiana, USA Anse-La-Rouge, St. Lucia, West lndies Birmingham, UK Nonvich, U K Cardiff, UK Glasgow, U K Brighton, UK London, U K London Leeds, UK Dublin B Baltimore, USA Baton Rouge, Louisiana, USA Baton Rouge Kansas, USA Kansas London, U K Dublin

(Yo positive)



No. of samples

Reference no.



I 529


20 25 21 25 29 9 21 66 I 6



80 80 80 80 80 400 503 14 53

4 4 4

11 7 (dogs kept as pets) 10 (no dogs present) 17.4 (swings) 39.1 (sandboxes) 5.2 28

146 30 30 23 23 250 36


4 4 5 17 Present study

18 14 14

12 12 19 Present study

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230 C. Holland et al.

Scand J Infect Dis 23 (1991)

The absence of toxocara ova in the faeces of pet dogs is not surprising as all samples came from regularly wormed dogs. In contrast the stray dogs had an infection rate of 6.2%. This compares well with 6.4 % reported from London (1 S ) , but is above that of 3 Yo recorded for a dog pound in Israel (16). In Louisiana pet dogs < 1 year of age had a prevalence of 27.3% compared with 2% for those > 1 year old while strays (all > 1 year old) had a prevalence of 12% (14). The prevalence of toxocara ova in street specimens did not differ significantly from that of the stray dogs. 13.3 Yo of samples collected from residential streets in Leeds contained toxocara ova (17). It appears that there is wide variation in the level of toxocara infestation of dogs by adult worms and also wide variation in the level of soil contamination by toxocara ova. It has been assumed that the route of infection is by ingestion of ova, most probably from soil. As eggs from Ascaris lumbricoides have been found in a number of household sites, including house dust (20), household dust was examined as a potential source of toxocara infection. However, no ova were found. This, and the finding of viable ova in so many soil samples, makes it likely that soil and not dust is the usual immediate source of infection.

ACKNOWLEDGEMENTS We thank Mr Peter Stafford and Miss Sandra McCune for technical assistance and the Toxocaral Reference Laboratory, London for toxocara ELISA titres.

REFERENCES 1. Taylor MRH, Keane CT, OConnor P, Mulvihill E, Holland C. The expanded spectrum of toxocaral

disease. Lancet 1: 692-699, 1988. 2. Mok CH. Visceral larva migrans: A discussion based on a review of the literature. Clin Pediatr 7: 565, 1968. 3. Glickman LT, Schantz PM. Epidemiology and pathogenesis of zoonotic toxocariasis. Epidemiol Rev 3: 230-250, 198 1. 4. Borg DA, Woodruff AW. Prevalence of infective ova of Toxocara species in public places. Br Med J 4: 470-472, 1973. 5. Snow KR, Ball SJ, Bewick JA. Prevalence of Toxocara species eggs in the soil of five east London parks. Vet Rec 120: 66-67, 1987. 6. Allen AHV, Ridley DS. Further observations on the formylether concentration technique for faecal parasites. J Clin Pathol 23: 545-546, 1970. 7. De Savigny DH, Voller A, Woodruff AW. Serological diagnosis by enzyme immunoassay. J Clin Pathol 32: 284-288. 1979. 8. Kazacos KR. Improved method of recovering ascarid and other helminth eggs from soil associated with epizootics and during survey studies. Am J Vet Res 44: 896-900, 1983. 9. Josephs DH, Bhinder P, Thompson AR. The prevalence of toxocara infection in a child population. Public Health 95: 273-275, 1981. 10. Woodruff AW, De Savigny DM, Jacobs DE. Study of toxocaral infection in dog breeders. Br Med J 2: 1747, 1978. 1 1 . Thompson DE, Bundy DAP, Cooper ES, Schantz PM. Epidemiological characteristics of Toxocara canis zoonotic infection of children in a Carribean community. Bull WHO 6 4 283-290, 1986. 12. Dada BJO, Lindquist WD. Prevalence of Toxocara sp. eggs in some public grounds and highway rest areas in Kansas. J Helminthol 53: 145-146, 1979. 13. Glickman LT, Magnaval JF, Domanski LM, Shofer FS, Lauria SS, Gottstein B, Brochier B. Visceral larva migrans in French adults: a new disease syndrome? Am J Epidemiol 125: 1019-1034, 1987. 14. Smith RE, Hagstad HV, Beard GB. Visceral larva migrans: A risk assessment in Baton Rouge, Louisiana. Int J Zoonos 1 1 : 189-194, 1984. 15. Oldham JN. Observations on the incidence of Toxocara and Toxascaris in dogs and cats from the London area. J Helminthol 39: 251-256, 1965. 16. Gross EM, Zeitan R, Tovak V. Toxocara canis infection in dogs in Beersheba, Israel. J Helminthol 58: 139-141, 1984.

Scand J Infect Dis23 (1991)

To.uocara untiDodiic>.$arrd tosocam m i i r e s

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17. Read MA, Thompson RCA. Prevalence of Toxocara canis and Toxascaris Leonina ova in dog faeces deposited on the streets of Leeds. J Helminthol 50: 95-96, 1976. 18. Childs JE. The prevalence of Toxocara species ova in backyards and gardens of Baltimore. Maryland. Am J Public Health 75: 1092-1094, 1985. 19. Pegg EJ. Dog roundworms and public health. Vet Rec 97: 78, 1975. 20. Crompton DWT, Nesheim MC, Pawlowski ZS. Ascariasis and its prevention and control. London, New York and Philadelphia: Taylor and Francis, 1989.

ISSSI-7. VILth International Symposium on Staphylococci and Staphylococcal Infections. June 29- July 3, 1992, Djuro, Stockholm, Sweden The symposium will be held in the Stockholm Archipelago. For further information and to receive second announcement and call for papers (scheduled for the autumn 1991) please contact:

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Families, parks, gardens and toxocariasis.

Toxocara canis antibody titres were measured in members of 30 families. 73/140 (52.1%) family members were seropositive for T. canis at a dilution gre...
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