Public Health (1991), 105, 335-3~39
© The Society of Public Health, 1991
The P r e v a l e n c e of T o x o c a r a Canis Ova in Soil S a m p l e s f r o m Parks and Gardens in the London Area S. H. Gillespie, M. Pereira and A. Ramsay Department of Medical Microbiology, Royal Free Hospital School of Medicine, Rowland Hill St, London NW3 2QG
Toxocara canis is an ascarid parasite of the dog. Human infection is acquired when ova of T. canis are ingested. Parks and play areas contaminated with dog faeces are recognised as potential sources of infection. Five hundred and twenty one soil samples were examined from fifteen parks and gardens in the greater London area to establish the prevalence of soil contamination in those facilities. Samples were examined using a magnesium sulphate floatation method. T. canis ova were found in 6.3% of the samples. Positive samples were commonly found in lawns, playing fields and children's play areas. The authors believe that this may constitute a significant health risk, particularly to children.
Introduction Toxocara canis, an ascarid parasite of the dog, is thought to be the main species of Toxocara responsible for h u m a n toxocariasis.
Y o u n g dogs may be infected by ingesting embryonated eggs. The eggs hatch in the stomach and second stage larvae (L2) penetrate the intestinal wall, proceeding on a liver-heart-lung migration characteristic of ascarid parasites. Larvae are coughed up and swallowed, developing into adult worms in the small intestine. In older dogs development from the L 2 larval stage is blocked and larvae migrate throughout the tissues before becoming dormant. During the sixth week of gestation the encysted larvae are activated and migrate transplacentally to infect the pups. ~ Infective larvae are also excreted in the bitch's milk. As a result almost all pups are infected perinatally and excrete eggs by the age of four weeks. 2 Adult worms are usually expelled by the age of six months. Once passed in canine faeces, T. eanis ova must undergo a period of development in the soil for 10-14 days before they become infective. Toxocara ova remain viable in the soil for more than two years. H u m a n infection is acquired by ingestion o f fully embryonated ova. As in the dog, the hatched larvae penetrate the intestinal wall and proceed on a liver-heart-lung migration. However, in the h u m a n host, T. canis L 2 larvae cannot develop into the adult stage but continue to migrate throughout the body. It is the inflammatory response to migrating larvae and their excretory products which is responsible for the clinical symptoms of toxocariasis. Seroprevalence rates in adults greater than the normal population can be found in those occupationally exposed to dogs such as dog breeders, 3 animal hospital employees, 4 and hydatid control officers. 5 A case-control study indicated that patients with ocular toxocariasis were more likely to own a dog. The relationship was especially strong if a puppy had been acquired in the year before s y m p t o m s developed. 6 Correspondence to: Dr S. H. Gillespie
336
S . H . Gillespie et al.
The burden of morbidity from toxocariasis falls on young children whose poor hand hygiene puts them at increased risk o f geo-helminth infections. 7 The longevity of Toxocara ova in soil means that public parks which are heavily fouled by dogs may be an important source of infection for children living in an urban environment. An increased public awareness o f the health risks posed by such amenities and the concern o f some local authorities has led to several surveys being conducted in recent years to assess the risk prevalence o f T. canis contamination. We report the results of such a survey taken in 15 public parks in the greater L o n d o n area. Materials and Methods
Fifteen surveys were performed in public parks and gardens in the greater London area (London NI, SWI, W2, SW5, SE5, SE10, Twickenham and Sutton, Surrey). At least 50 g of soil was collected and the position o f sampling marked on a site map. Five hundred and twenty one soil samples were examined using a modification of the method o f Quinn et al. 8 Approximately 25 g o f the soil sample was passed through a sieve (pore size 4 m m ) to remove stones, grass and other solid objects. 100ml o f 0.0025% aqueous Tween 80 solution (BDH Analar, England) was added to each sample as a wetting agent before being homogenised in a heavy duty laboratory homogeniser (Silverson Machines Ltd) for five minutes. Samples were then transferred to two 50ml round-bottomed centrifuge tubes and centrifuged at 2,000rpm for l0 minutes. The supernatant was discarded and the sediment resuspended in saturated magnesium sulphate solution (BDH Analar). This mixture was centrifuged again at 2,000 rpm for 10 minutes. The centrifuge tubes were topped up with more magnesium sulphate solution to form a positive meniscus. A coverslip was placed on top of the tube and left for five minutes. The coverslip was then trajasferred to a glass slide and examined microscopically for the presence o f T o x o c a r a ova using the x 10 objective. T o x o e a r a canis ova were identified on the basis o f size, as measured by a calibrated eyepiece graticule, and their characteristic morphology. Results
O f the 521 samples examined, 33 (6.3%) were found to contain ova o f T o x o c a r a canis. These results are summarised in Table I by geographic location. Three hundred and twenty seven of these samples were taken from parks and gardens in heavily built-up areas of London of which 21 samples (6.4%) were found to contain T. canis ova. The prevalence o f Toxocara ova in individual parks and gardens varied from 0-20%, although the sample size in some o f these parks and gardens was small. Fifteen positive samples (out o f 259) taken in public gardens were located in L o n d o n squares and six (out of 68) in open public parks. Using site maps, the location o f individual positive samples could be located. In gardens where access was restricted to owners o f neighbouring properties, nine positive samples out o f 129 (6.9%) were found in lawn areas and two positive out o f 61 (3.2%) in the shrubbery. Two positive samples (out of 42) were found in designated areas for dogs, two (out o f 64) in children's play areas and three (out o f 31) in open spaces. One hundred and ninety four samples were taken from parks in Sutton. Twelve samples (6.2%) contained T. eanis ova. O f these, eight were from the grass verges of paths on the perimeter o f the park, three were from a children's play area and one from the edge of a playing field.
337
Toxocara Contamination o f Soil Table I
Prevalence of T. canis contamination of public parks and gardens in the London area
Locality of survey London N1 London SW1 London W2 London SW5 London SE5 London SE10 London (Twickenham) Sutton, Surrey Total
Number of samples taken
Number of samples positive
Percentage of samples positive
8 229 12 30 10 22 16
1 14 0 1 2 1 2
12.5 6.1 N/A 3.3 20.0 4.5 12.5
194 521
12 33
6.2 6.3
Discussion
H u m a n to×ocariasis is a c o m m o n infection in the U K . In a survey of healthy adults from London, 2.6% had serological evidence o f infection with Toxocara sp. 9 Similar seroprevatence has been reported f r o m other developed countries. I° However, these data underestimate the n u m b e r o f cases o f h u m a n toxocariasis as most infections are acquired in childhood. F o r example, a survey o f children in Bedford found that 14.6% had serological evidence of toxocariasis.11 Seropositivity is strongly associated with a history of pica and p u p p y ownership.t2 In the U S A positive serology was found m o r e c o m m o n l y in black than in white children, but this was entirely due to differences in socio-economic classJ 3 Very high seroprevalence was found in children in St Lucia, where 86% had antibodies to Toxocara sp. 14 This was associated with a high prevalence o f Toxocara contamination o f soil in a climate which favoured the transmission o f geo-helminthic parasites. In experimental models o f infection, the immune response to Toxocara infection varies, depending on the size and frequency of the infecting dose. Liver trapping of parasites occurs when the infective dose is large or repeated infections take place. When the infecting dose is small, the antibody response is correspondingly small and liver trapping does not occur. This has led to the hypothesis that ocular toxocariasis is associated with infection with a small n u m b e r o f larvae. It is i m p o r t a n t therefore that the low-level exposure most likely to occur in parks is avoidedJ 5 There have been only a few published reports of environmental contamination with Toxocara in the U K . and these show conflicting results. A survey carried out in L o n d o n and other U K cities during the early 1970s demonstrated that 24.4% o f 800 samples had ova o f Toxocara spJ 6 M o r e recently, a survey o f five East L o n d o n parks found that 332 out o f 503 samples contained ova. 17The study reported here shows 6.3% of samples contained ova of T. canis in a consistent pattern in parks across London. This is much lower than previous surveys, although the method used in this study has been shown to provide the best recovery rate for Toxocara ova in c o m p a r a t i v e studies. 8 Soil surveys f r o m other centres show highly variable results, summarised in Table II. 18 2~ This demonstrates that the prevalence o f soil contamination in the London area may be
338
S. H. Gillespie et al. Table II
Prevalence of soil contamination by eggs of Toxocara canis in other centres
Country
Locality
UK (this study) UK ~7 UK ~6 Canada t8 Canada ~9 USA2° USA 2~ St Lucia ~4
London London London etc. Montreal Halifax Kansas Baltimore Anse-le-Raye
No. of samples
Prevalence (%)
521 503 800 43 567 236 146 41
6.4 66 24 32 2 15 11 19
14'16'17'18'19'29"21See references.
lower than previous reports have suggested and lower than in many other cities. However, this study showed that there was a risk of acquiring toxocariasis in almost all the parks surveyed. It also demonstrates that infective ova could be found in children's play areas. The humoral immune response to Toxocara by non-canid hosts appears to show a linear relationship with the number of ova ingested. Ocular disease is associated with the absence of liver trapping of larvae and low antibody concentrations in the host.~5 Therefore, the low level ingestion of T. canis ova likely to occur in parks may be an important risk factor for acquisition of ocular toxocariasis. Surveys, such as the one described in this paper, are of limited value in indicating the degree of risk to individuals or populations because the size of the infecting dose and the percentage of seroconverters who progress to have clinical disease is not known. A high prevalence of soil con'tamination and poor sanitation are associated with high seroprevalence in children. ~4 This work indicates that measures to control dog fouling are required to reduce the risk of Toxocara transmission. It also provides a baseline from which the effect of control measures may be monitored. Since T. canis ova can remain viable for more than two years, control o f toxocariasis is a long-term commitment. 'Poop-scoops', 'doggy loos', and fencing of play areas have all been suggested to reduce the risk of transmission, but the benefit of these methods has not been evaluated. Further surveys are, thus, necessary, to study the effect of such control measures on the prevalence of soil contamination. References
1. Sprent, J. F. A. (1958). Observations of the development of Toxocara canis (Werner 1782) in the dog. Parasitology, 48, 184-209. 2. Scothorn, M.W., Koutz, F. R. & Groves, H.F. (1965). Perinatal Toxocara canis infection in pups. Journal of American Veterinary Medical Association, 146, 45-48. 3. Woodruff, A. W., de Savigny, D. H. and Jacobs, D. E. (1978). Study of Toxocaral infection in dog breeders. British Medical Journal, 4, 1747-1748. 4. Glickman, L.T. & Cypess, R.H. (1977). Toxocara infection in animal hospital employees. American Journal of Public Health, 67, 1193-1195. 5. Clemett, R.S. (1985). Toxocaral infection in hydatid control officers: diagnosis by enzyme immunoassay. New Zealand Journal of Medicine, 98, 737-739. 6. Schantz, P. M., Weis, P. E., Pollard, Z. F. and White, M. C. (1980). Risk factors for ocular larva migrans: a case control study. American Journal of Public Health, 70, 1269-1272.
Toxocara Contamination o f Soil
339
7. Bundy, D. A. P., Thompson, D. E., Robertson, B. D. & Cooper, E. S. (1987). Age-relationships of Toxocara canis seropositivity and geohelminthic infection prevalence in two communities in St Lucia West Indies. Tropical Medical Parasitology, 38, 309-312. 8. Quinn, R., Smith, H.V., Bruce, R. G. & Girdwood, R.W. (1980). Studies on the incidence of Toxocara and Toxascaris spp., in the environment. 1. A comparison of floatation procedures for recovering Toxocara sp., from the soil, Journal of Hygiene (London), 84, 83 89. 9. de Savigny, D. H., VoUer, A. & Woodruff, A. W. (1979). Toxocariasis: Serological diagnosis by enzyme immunoassay. Journal of Clinical Pathology, 32, 284-288. 10. Nicholas, W.L., Stewart, A.C. & Walker, J.C. (1986). Toxocariasis: a serological survey of blood donors in the Australian Capital Territory. Transactions of the Royal Society of Tropical Medicine and Hygiene, 80, 217-221. 11. Josephs, D. S., Bhinder, P. & Thompson, A. R. (1981), The prevalence of Toxocara infection in a child population. Public Health, 95, 273-275. 12. Marmao, M., Glickman, L., Shofer F. et al. (1987). Toxocara canis infection of children: epidemiological and neuropsychological findings. American Journal of Public Health, 77, 554559. 13. Worley, G., Green, J. A., Frothingham, T. E. et al. (1984). Toxocara canis infection: clinical and epidemiological associations with seropositivity in kindergarten children. Journal of Infectious Diseases, 149(4), 591-597. 14. Thompson, D.E., Bundy, D. A. P., Cooper, E.S. & Schantz, P.M. (1986). Epidemiological characteristics of Toxocara canis zoonotic infection of children in a Caribbean community. Bulletin of the World Health Organisation, 64(2), 283-290. 15. Schantz, P. M. (1989). Toxocara larva migrans now. American Journal of Tropical Medicine and Hygiene, 41, Suppl. 21-34. 16. Borg, O. A. & Woodruff, A. W. (1973). Prevalence of infective ova of Toxocara species. British Medical Journal, 4, 470-472. 17. Snow, K. R., Ball, S. J. & Bewick, J. A. (1987). Prevalence of Toxocara species in the soil of five east London parks. Veterinary Record, 120, 66~7. 18. Ghadirian, E., Veins, P., Strykowski, H. & Dubreuil, F. (1987). Epidemiology of Toxocariasis in the Montreal area. Canadian Journal of Public Health, 67, 495-498. 19. Gualazzi, D. A., Embil, J. A. & Pereira, L. H. (1986). Prevalence of helminth ova in recreational areas of peninsular Halifax, Nova Scotia. Canadian Journal of Public Health, 77, 147-151. 20. Dada, B. J. O. & Lindquist, W. D. (1979). Prevalence of Toxocara sp eggs in some public grounds and highway rest areas in Kansas. Journal of Helminthology, 53, 145-146. 21. Childs, J.E. (1985). The prevalence of Toxocara species ova in backyards and gardens in Baltimore, Maryland. American Journal of Public Health, 75, 1092-1093.
© The Society of Public Health, 1991
The P r e v a l e n c e of T o x o c a r a Canis Ova in Soil S a m p l e s f r o m Parks and Gardens in the London Area S. H. Gillespie, M. Pereira and A. Ramsay Department of Medical Microbiology, Royal Free Hospital School of Medicine, Rowland Hill St, London NW3 2QG
Toxocara canis is an ascarid parasite of the dog. Human infection is acquired when ova of T. canis are ingested. Parks and play areas contaminated with dog faeces are recognised as potential sources of infection. Five hundred and twenty one soil samples were examined from fifteen parks and gardens in the greater London area to establish the prevalence of soil contamination in those facilities. Samples were examined using a magnesium sulphate floatation method. T. canis ova were found in 6.3% of the samples. Positive samples were commonly found in lawns, playing fields and children's play areas. The authors believe that this may constitute a significant health risk, particularly to children.
Introduction Toxocara canis, an ascarid parasite of the dog, is thought to be the main species of Toxocara responsible for h u m a n toxocariasis.
Y o u n g dogs may be infected by ingesting embryonated eggs. The eggs hatch in the stomach and second stage larvae (L2) penetrate the intestinal wall, proceeding on a liver-heart-lung migration characteristic of ascarid parasites. Larvae are coughed up and swallowed, developing into adult worms in the small intestine. In older dogs development from the L 2 larval stage is blocked and larvae migrate throughout the tissues before becoming dormant. During the sixth week of gestation the encysted larvae are activated and migrate transplacentally to infect the pups. ~ Infective larvae are also excreted in the bitch's milk. As a result almost all pups are infected perinatally and excrete eggs by the age of four weeks. 2 Adult worms are usually expelled by the age of six months. Once passed in canine faeces, T. eanis ova must undergo a period of development in the soil for 10-14 days before they become infective. Toxocara ova remain viable in the soil for more than two years. H u m a n infection is acquired by ingestion o f fully embryonated ova. As in the dog, the hatched larvae penetrate the intestinal wall and proceed on a liver-heart-lung migration. However, in the h u m a n host, T. canis L 2 larvae cannot develop into the adult stage but continue to migrate throughout the body. It is the inflammatory response to migrating larvae and their excretory products which is responsible for the clinical symptoms of toxocariasis. Seroprevalence rates in adults greater than the normal population can be found in those occupationally exposed to dogs such as dog breeders, 3 animal hospital employees, 4 and hydatid control officers. 5 A case-control study indicated that patients with ocular toxocariasis were more likely to own a dog. The relationship was especially strong if a puppy had been acquired in the year before s y m p t o m s developed. 6 Correspondence to: Dr S. H. Gillespie
336
S . H . Gillespie et al.
The burden of morbidity from toxocariasis falls on young children whose poor hand hygiene puts them at increased risk o f geo-helminth infections. 7 The longevity of Toxocara ova in soil means that public parks which are heavily fouled by dogs may be an important source of infection for children living in an urban environment. An increased public awareness o f the health risks posed by such amenities and the concern o f some local authorities has led to several surveys being conducted in recent years to assess the risk prevalence o f T. canis contamination. We report the results of such a survey taken in 15 public parks in the greater L o n d o n area. Materials and Methods
Fifteen surveys were performed in public parks and gardens in the greater London area (London NI, SWI, W2, SW5, SE5, SE10, Twickenham and Sutton, Surrey). At least 50 g of soil was collected and the position o f sampling marked on a site map. Five hundred and twenty one soil samples were examined using a modification of the method o f Quinn et al. 8 Approximately 25 g o f the soil sample was passed through a sieve (pore size 4 m m ) to remove stones, grass and other solid objects. 100ml o f 0.0025% aqueous Tween 80 solution (BDH Analar, England) was added to each sample as a wetting agent before being homogenised in a heavy duty laboratory homogeniser (Silverson Machines Ltd) for five minutes. Samples were then transferred to two 50ml round-bottomed centrifuge tubes and centrifuged at 2,000rpm for l0 minutes. The supernatant was discarded and the sediment resuspended in saturated magnesium sulphate solution (BDH Analar). This mixture was centrifuged again at 2,000 rpm for 10 minutes. The centrifuge tubes were topped up with more magnesium sulphate solution to form a positive meniscus. A coverslip was placed on top of the tube and left for five minutes. The coverslip was then trajasferred to a glass slide and examined microscopically for the presence o f T o x o c a r a ova using the x 10 objective. T o x o e a r a canis ova were identified on the basis o f size, as measured by a calibrated eyepiece graticule, and their characteristic morphology. Results
O f the 521 samples examined, 33 (6.3%) were found to contain ova o f T o x o c a r a canis. These results are summarised in Table I by geographic location. Three hundred and twenty seven of these samples were taken from parks and gardens in heavily built-up areas of London of which 21 samples (6.4%) were found to contain T. canis ova. The prevalence o f Toxocara ova in individual parks and gardens varied from 0-20%, although the sample size in some o f these parks and gardens was small. Fifteen positive samples (out o f 259) taken in public gardens were located in L o n d o n squares and six (out of 68) in open public parks. Using site maps, the location o f individual positive samples could be located. In gardens where access was restricted to owners o f neighbouring properties, nine positive samples out o f 129 (6.9%) were found in lawn areas and two positive out o f 61 (3.2%) in the shrubbery. Two positive samples (out of 42) were found in designated areas for dogs, two (out o f 64) in children's play areas and three (out o f 31) in open spaces. One hundred and ninety four samples were taken from parks in Sutton. Twelve samples (6.2%) contained T. eanis ova. O f these, eight were from the grass verges of paths on the perimeter o f the park, three were from a children's play area and one from the edge of a playing field.
337
Toxocara Contamination o f Soil Table I
Prevalence of T. canis contamination of public parks and gardens in the London area
Locality of survey London N1 London SW1 London W2 London SW5 London SE5 London SE10 London (Twickenham) Sutton, Surrey Total
Number of samples taken
Number of samples positive
Percentage of samples positive
8 229 12 30 10 22 16
1 14 0 1 2 1 2
12.5 6.1 N/A 3.3 20.0 4.5 12.5
194 521
12 33
6.2 6.3
Discussion
H u m a n to×ocariasis is a c o m m o n infection in the U K . In a survey of healthy adults from London, 2.6% had serological evidence o f infection with Toxocara sp. 9 Similar seroprevatence has been reported f r o m other developed countries. I° However, these data underestimate the n u m b e r o f cases o f h u m a n toxocariasis as most infections are acquired in childhood. F o r example, a survey o f children in Bedford found that 14.6% had serological evidence of toxocariasis.11 Seropositivity is strongly associated with a history of pica and p u p p y ownership.t2 In the U S A positive serology was found m o r e c o m m o n l y in black than in white children, but this was entirely due to differences in socio-economic classJ 3 Very high seroprevalence was found in children in St Lucia, where 86% had antibodies to Toxocara sp. 14 This was associated with a high prevalence o f Toxocara contamination o f soil in a climate which favoured the transmission o f geo-helminthic parasites. In experimental models o f infection, the immune response to Toxocara infection varies, depending on the size and frequency of the infecting dose. Liver trapping of parasites occurs when the infective dose is large or repeated infections take place. When the infecting dose is small, the antibody response is correspondingly small and liver trapping does not occur. This has led to the hypothesis that ocular toxocariasis is associated with infection with a small n u m b e r o f larvae. It is i m p o r t a n t therefore that the low-level exposure most likely to occur in parks is avoidedJ 5 There have been only a few published reports of environmental contamination with Toxocara in the U K . and these show conflicting results. A survey carried out in L o n d o n and other U K cities during the early 1970s demonstrated that 24.4% o f 800 samples had ova o f Toxocara spJ 6 M o r e recently, a survey o f five East L o n d o n parks found that 332 out o f 503 samples contained ova. 17The study reported here shows 6.3% of samples contained ova of T. canis in a consistent pattern in parks across London. This is much lower than previous surveys, although the method used in this study has been shown to provide the best recovery rate for Toxocara ova in c o m p a r a t i v e studies. 8 Soil surveys f r o m other centres show highly variable results, summarised in Table II. 18 2~ This demonstrates that the prevalence o f soil contamination in the London area may be
338
S. H. Gillespie et al. Table II
Prevalence of soil contamination by eggs of Toxocara canis in other centres
Country
Locality
UK (this study) UK ~7 UK ~6 Canada t8 Canada ~9 USA2° USA 2~ St Lucia ~4
London London London etc. Montreal Halifax Kansas Baltimore Anse-le-Raye
No. of samples
Prevalence (%)
521 503 800 43 567 236 146 41
6.4 66 24 32 2 15 11 19
14'16'17'18'19'29"21See references.
lower than previous reports have suggested and lower than in many other cities. However, this study showed that there was a risk of acquiring toxocariasis in almost all the parks surveyed. It also demonstrates that infective ova could be found in children's play areas. The humoral immune response to Toxocara by non-canid hosts appears to show a linear relationship with the number of ova ingested. Ocular disease is associated with the absence of liver trapping of larvae and low antibody concentrations in the host.~5 Therefore, the low level ingestion of T. canis ova likely to occur in parks may be an important risk factor for acquisition of ocular toxocariasis. Surveys, such as the one described in this paper, are of limited value in indicating the degree of risk to individuals or populations because the size of the infecting dose and the percentage of seroconverters who progress to have clinical disease is not known. A high prevalence of soil con'tamination and poor sanitation are associated with high seroprevalence in children. ~4 This work indicates that measures to control dog fouling are required to reduce the risk of Toxocara transmission. It also provides a baseline from which the effect of control measures may be monitored. Since T. canis ova can remain viable for more than two years, control o f toxocariasis is a long-term commitment. 'Poop-scoops', 'doggy loos', and fencing of play areas have all been suggested to reduce the risk of transmission, but the benefit of these methods has not been evaluated. Further surveys are, thus, necessary, to study the effect of such control measures on the prevalence of soil contamination. References
1. Sprent, J. F. A. (1958). Observations of the development of Toxocara canis (Werner 1782) in the dog. Parasitology, 48, 184-209. 2. Scothorn, M.W., Koutz, F. R. & Groves, H.F. (1965). Perinatal Toxocara canis infection in pups. Journal of American Veterinary Medical Association, 146, 45-48. 3. Woodruff, A. W., de Savigny, D. H. and Jacobs, D. E. (1978). Study of Toxocaral infection in dog breeders. British Medical Journal, 4, 1747-1748. 4. Glickman, L.T. & Cypess, R.H. (1977). Toxocara infection in animal hospital employees. American Journal of Public Health, 67, 1193-1195. 5. Clemett, R.S. (1985). Toxocaral infection in hydatid control officers: diagnosis by enzyme immunoassay. New Zealand Journal of Medicine, 98, 737-739. 6. Schantz, P. M., Weis, P. E., Pollard, Z. F. and White, M. C. (1980). Risk factors for ocular larva migrans: a case control study. American Journal of Public Health, 70, 1269-1272.
Toxocara Contamination o f Soil
339
7. Bundy, D. A. P., Thompson, D. E., Robertson, B. D. & Cooper, E. S. (1987). Age-relationships of Toxocara canis seropositivity and geohelminthic infection prevalence in two communities in St Lucia West Indies. Tropical Medical Parasitology, 38, 309-312. 8. Quinn, R., Smith, H.V., Bruce, R. G. & Girdwood, R.W. (1980). Studies on the incidence of Toxocara and Toxascaris spp., in the environment. 1. A comparison of floatation procedures for recovering Toxocara sp., from the soil, Journal of Hygiene (London), 84, 83 89. 9. de Savigny, D. H., VoUer, A. & Woodruff, A. W. (1979). Toxocariasis: Serological diagnosis by enzyme immunoassay. Journal of Clinical Pathology, 32, 284-288. 10. Nicholas, W.L., Stewart, A.C. & Walker, J.C. (1986). Toxocariasis: a serological survey of blood donors in the Australian Capital Territory. Transactions of the Royal Society of Tropical Medicine and Hygiene, 80, 217-221. 11. Josephs, D. S., Bhinder, P. & Thompson, A. R. (1981), The prevalence of Toxocara infection in a child population. Public Health, 95, 273-275. 12. Marmao, M., Glickman, L., Shofer F. et al. (1987). Toxocara canis infection of children: epidemiological and neuropsychological findings. American Journal of Public Health, 77, 554559. 13. Worley, G., Green, J. A., Frothingham, T. E. et al. (1984). Toxocara canis infection: clinical and epidemiological associations with seropositivity in kindergarten children. Journal of Infectious Diseases, 149(4), 591-597. 14. Thompson, D.E., Bundy, D. A. P., Cooper, E.S. & Schantz, P.M. (1986). Epidemiological characteristics of Toxocara canis zoonotic infection of children in a Caribbean community. Bulletin of the World Health Organisation, 64(2), 283-290. 15. Schantz, P. M. (1989). Toxocara larva migrans now. American Journal of Tropical Medicine and Hygiene, 41, Suppl. 21-34. 16. Borg, O. A. & Woodruff, A. W. (1973). Prevalence of infective ova of Toxocara species. British Medical Journal, 4, 470-472. 17. Snow, K. R., Ball, S. J. & Bewick, J. A. (1987). Prevalence of Toxocara species in the soil of five east London parks. Veterinary Record, 120, 66~7. 18. Ghadirian, E., Veins, P., Strykowski, H. & Dubreuil, F. (1987). Epidemiology of Toxocariasis in the Montreal area. Canadian Journal of Public Health, 67, 495-498. 19. Gualazzi, D. A., Embil, J. A. & Pereira, L. H. (1986). Prevalence of helminth ova in recreational areas of peninsular Halifax, Nova Scotia. Canadian Journal of Public Health, 77, 147-151. 20. Dada, B. J. O. & Lindquist, W. D. (1979). Prevalence of Toxocara sp eggs in some public grounds and highway rest areas in Kansas. Journal of Helminthology, 53, 145-146. 21. Childs, J.E. (1985). The prevalence of Toxocara species ova in backyards and gardens in Baltimore, Maryland. American Journal of Public Health, 75, 1092-1093.
