TOXOPLASMOSIS IN GOATS IN SOUTHERN ONTARIO - A PUBLIC HEALTH HAZARD? 1. R. Tizard, M. Carrington and C. H. Lai* INTRODUCTION
ALTHOUGH Toxoplasma gondii only causes occasional disease in man, infection by this organism, as shown by the prevalence of serum antibodies may be relatively common (8). For example, up to 40% of the population of southern Ontario may possess anti-Toxoplasma antibodies as detected by the Sabin-Feldman dye test (11). The source of this human infection is not clear. While a small percentage of affected individuals acquire infection in utero, most cases are probably contracted either through the ingestion of grossly undercooked or raw meat, or by the accidental ingestion of ocysts shed by infected cats (3). Unfortunately, the relative importance of these two routes in southern Ontario is unknown. While surveying domestic animals in southern Ontario for serological evidence of Toxoplasma infection, it was observed that a very high percentage of the goat sera tested reacted positively in the Sabin-Feldman dye test. This was investigated further and this paper presents the results of a survey of goat sera for the presence of anti-Toxoplasma antibodies and a discussion of these results in relation, not only to their public health significance, but also to the epidemiology of this infection. MATERIALS
AND
METHODS
Samples Sera from 399 goats were tested. These samples were obtained from two sources: 198 samples were obtained from animals in 20 selected flocks located within 50 miles of Guelph. Samples were taken from approximately ten animals in each flock. These animals were selected in an attempt to ensure that both sexes and as wide a range of age groups as possible were tested. At the time of sampling owners were questioned concerning the health of the herd, their management practices, the presence of cats and other animals, the distribution of their products (meat
*Toxoplasmosis
Diagnostic Laboratory, Department of Veterinary Microbiology and Immunology, Ontario Veterinary College, University of
Guelph, Guelph, Ontario NIG 2W1.
CAN. VET. JOUR., vol. 18, no. 10, October, 1977
and milk) and the health of the owners and of their family. The remaining 201 serum samples were obtained from female goats through the courtesy of Agriculture Canada. These samples had been submitted for brucellosis testing to the Federal Animal Pathology Laboratory, Guelph. No information, apart from their age, was available concerning these animals.
Testing procedure Serum samples were frozen at -20°C immediately upon receipt. They were inactivated by incubation at 56°C for 45 minutes immediately prior to testing. The Sabin-Feldman dye test was conducted in a standard manner using human accessory factor (9) and all goat sera were tested at a dilution of 1:16. The samples obtained from the selected farms were also titrated using fourfold dilutions to a final dilution of 1:1024. RESULTS
Of the 399 goat sera tested, 252 (63.1%) gave a positive reaction at a dilution of 1:16 or greater. In the samples obtained from selected farms, 55% of animals tested were positive while in those samples submitted for Brucella serology 71.1% were positive. This difference may be explained on the basis of the different age distributions within each sample population. For example, very few of the samples submitted for Brucella serology were from goats less than one year of age. As might be anticipated the prevalence of positive reactions varied with the age of the goat population (Figure 1). For example, of goats less than one year of age, 38/66 (57%) were seropositive, this dropped to 42% (28/67) of one year old animals, but thereafter climbed progressively to reach 85% (42/49) in four year old animals. The drop in prevalence during the first year of life may be a reflection of a loss of maternal immunity. A similar phenomenon is observed in humans (11). Because of the influence of age all further analyses were first adjusted to account for any differences in the age distribution of sample populations. There were no differences in the prevalence ,74
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FIGURE 1. The distribution of positive serological reactions to Toxoplasma gondii as a function of the age of goats. The fractions indicate the number of positive animals out of the number tested.
of positive reactions between the sexes. Thus male goats were 51.4% positive while female goats were 51.2% positive. When the samples taken from selected farms were investigated, the only factor which appeared to exert any direct influence on the percentage of positive reactions was the age distribution of the population sampled. No significant relationships emerged between the prevalence of positive reactions, the size of the goat herd, the major goat breed kept, the number of cats on the farm (most farms had cats), a history of abortions or stillbirths, or the occurrence of caseous lymphadenitis (Table I). No significant association was established between toxoplasmosis in goats and illness in humans although interestingly, the husband of one goat owner, was hospitalized with a suspected toxoplasma myocarditis during the course of this study. The distribution of antibody titers within the selected population (Figure 2) showed no unusual features and, unlike the distribution of titers within the human population was not biomodal (10). DISCUSSION These results are of interest from several
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Firstly, because the prevalence of positive reactions to Toxoplasma found in goats aspects.
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CANADIAN VETERINARY JOURNAL ern Ontario and found nine
(52.9%) to be positive for toxoplasmosis (6). 60 The growing market for "natural foods" has * Humans led to an increasing demand for unpasteurized & 50 goat's milk for human consumption. In addi= 40 tion, the relatively small volumes of milk produced and the small number of farms in0 30 volved have combined to make it difficult for It 20 producers to get their milk pasteurized. For these reasons, it became apparent while ques10 tioning goat owners that a high proportion of the milk produced by dairy goats is consumed 0 or the owner's friends. Unfor'YJ6 1A6 1/64 1/256 2i1024 by the owner is it well tunately, recognized that unpasteurTiter ized goat's milk may serve as a source of FIGURE 2. The distribution of antibody titers Toxoplasma infection for humans (7). It is in 175 goats from selected farms compared with therefore not unlikely that the consumption the distribution observed in humans in southern of unpasteurized goat's milk may represent a Ontario. Human data derived from Reference 10. significant public health hazard. Goat meat in contrast, because of its "relatively strong flavor", appears to be generally well cooked is considerably higher than that seen in most in this country and if this is indeed the case, other species of domestic animal in southern then it is unlikely to represent a significant Ontario, secondly, because of a growing ten- source of infection. dency to consume unpasteurized goat's milk in Finally, in spite of the high prevalence of the interests of "health", and finally, because antibodies to this organism reported here we it is apparent that the occurrence of positive have not found it to be a significant clinical serological reactions in goats is not inevitably problem in goats. For this reason we would associated with severe clinical problems. disagree with the comments on this condition Unpublished data indicate that the preva- in Blood and Henderson (1). We consider lence of positive serological reactions to T. the disease to be enzootic in these animals in gondii among the domestic animals of south- this region and that any attempt to eradicate ern Ontario varies from 9% in horses, and 16% or even reduce the prevalence of this infection in cattle to 44% in swine and 65% in sheep. It by slaughter would be futile, at least until the is apparent therefore that sheep and goats precise source of infection of these animals may become infected much more frequently can be ascertained. than the other animals. The reasons for this are not clear. Our current understanding of SUMMARY the epidemiology of toxoplasmosis would suggest that herbivores acquire infection through With the Sabin-Feldman dye test, 252 out feline oocysts shed on grass (3). However, of 399 goat sera gave positive reactions for goats tend to browse rather than graze and antibodies to Toxoplasma gondii. This result while they are capable of cropping grass very is of significance from the public health aspect close to the ground, they will only do so if no particularly in view of the increasing conother food is available (8). They are also sumption of raw goat's milk and it is also of somewhat fastidious eaters and are therefore considerable epidemiological interest. unlikely to knowingly consume feline fecal material or dead mice. In view of this we RESUME' believe it possible that transmission of Toxoplasma to these animals might be by a comL'utilisation de l'epreuve au bleu de mepletely different and so far unidentified route. thylene de Sabin-Feldman a permis de deceler Toxoplasmosis also appears to be highly prev- des anticorps contre Toxoplasma gondii, dans alent in goats in other parts of the world. 252 des 399 echantillons de serum caprin Thus in Egypt 47% of goats are positive (5), eprouves a cette fin. Ce resultat s'avere signiand in Turkey 52% (13). In the U.S.A. the ficatif en ce qui concerne la sante publique, prevalence varies, it has been reported to be surtout si l'on tient compte de l'accroissement 43% (28/65) (2) in central New York and to actuel de la consommation de lait cru de be 27% (21/77) in northern California (12). chevre; il revet aussi un interet epidemioQuinn and McCraw tested 17 goats in south- logique considerable. 70
aI
Goats
FL1n .Fh
276
TOXOPLASMOSIS
7. RIEMNANN, H. P., M. E. MEYER, J. H. THEIS, G. KELSO and D. E. BEHYMIER. Toxoplasmosis in an infant fed unpasteurized goat's milk. J. Pediatrics 87: 573-576. 1975. 8. SABIN, A. B. Toxoplasmosis: Current status and unresolved problems. Introductory remarks. Am. J. trop. Med. Hyg. 2: 360-364. 1953. 9. SABIN, A. B. and H. A. FELDMAN. Dyes as microchemical indicators of a new immunity phenomenon affecting a protozoan parasite (Toxoplasma). Science 108: 660663. 1948. 10. TIZARD, I. R., S. S. CHAUHAN and C. H. LAI. The prevalence and epidemiology of toxoplasmosis in Ontario. J. Hyg., Camb. 78: 275-282. 1977. 11. TIZARD, I. R., P. J. QUINN and N. A. FISH. Some observations on the epidemiology of toxoplasmosis in Canada. J. Hyg., Camb. 77: 11-21. 1976. 12. VANDERWAGEN, L. C., D. E. BEHYMER, H. P. RIEMANN and C. E. FRANTI. A survey for Toxoplasma antibodies in northern California livestock and dogs. J. Am. vet. med. Ass. 164: 1034-1037. 1974. 13. WEILAND, G. and W. DALCHOW. Toxoplasma-Infektionen bei Haustieren in der Turkei. Berl. Munch. tierarztl. Wschr. 83: 6568. 1970.
ACKNOWLEDGNIENTS
This work was supported by the Ontario Ministry of Health. REFERENCES 1. BLOOD, D. C. and J. A. HENDERSON. Veterinary Medicine, 4th Edition. London: Balliere, Tindall. 1974. 2. FELDMAN, H. A. and L. T. MILLER. Sero-
logical study of toxoplasmosis prevalence. Am. J. Hyg. 64: 320-335. 1956. 3. FRENKEL, J. K. Toxoplasmosis. In Parasite Life Cycle, Pathology, and Immunology in the Coccidia. D. M. Hammond and P. L. Long, Editors. Baltimore: University Park Press. 1973. 4. HAFEZ, E. S. E. and J. P. SCOTT. The behaviour of sheep and goats. In The Behaviour of Domestic Animals. E. S. E. Hafe7, Editor. London: Balliere, Tindall, and Cox. 1962. 5. MARONPOT, R. R. and B. A. M. BOTROS. Toxoplasma serologic survey on man and domestic animals in Egypt. J. Egypt. publ. Hlth Ass. 47: 58-67. 1972.
6. QUINN, P. J. and B. M. MCCRAW. Current status of Toxoplasma and toxoplasmosis. A review. Can. vet. J. 13: 247-262. 1972.
SCHERING AWARD FOR VETERINARY STUDENTS Schering awards are offered to senior students in each of the three Canadian Veterinary Colleges. Three $100 awards will be available to each college.
3. 4.
RULES 1. Eligibility. The competition is limited to students in their final year at a Canadian veterinary college. 2. The awards will be given for the best case reports, preferably of 300-1,000 words, written in a form acceptable for publication in the Canadian Veterinary Journal.
277
5.
6.
Please consult "Instructions to Authors" and recent issues of the Journal for form. Entries will be accepted in either English or French. A committee from each College will be responsible for selecting the ten best case reports which will be judged by the Editorial Board of the Canadian Veterinary Medical Association. The awards will be presented at a suitable function. The Journal reserves the right to publish the prize-winning papers subject to the usual editorial procedures.
ALTHOUGH Toxoplasma gondii only causes occasional disease in man, infection by this organism, as shown by the prevalence of serum antibodies may be relatively common (8). For example, up to 40% of the population of southern Ontario may possess anti-Toxoplasma antibodies as detected by the Sabin-Feldman dye test (11). The source of this human infection is not clear. While a small percentage of affected individuals acquire infection in utero, most cases are probably contracted either through the ingestion of grossly undercooked or raw meat, or by the accidental ingestion of ocysts shed by infected cats (3). Unfortunately, the relative importance of these two routes in southern Ontario is unknown. While surveying domestic animals in southern Ontario for serological evidence of Toxoplasma infection, it was observed that a very high percentage of the goat sera tested reacted positively in the Sabin-Feldman dye test. This was investigated further and this paper presents the results of a survey of goat sera for the presence of anti-Toxoplasma antibodies and a discussion of these results in relation, not only to their public health significance, but also to the epidemiology of this infection. MATERIALS
AND
METHODS
Samples Sera from 399 goats were tested. These samples were obtained from two sources: 198 samples were obtained from animals in 20 selected flocks located within 50 miles of Guelph. Samples were taken from approximately ten animals in each flock. These animals were selected in an attempt to ensure that both sexes and as wide a range of age groups as possible were tested. At the time of sampling owners were questioned concerning the health of the herd, their management practices, the presence of cats and other animals, the distribution of their products (meat
*Toxoplasmosis
Diagnostic Laboratory, Department of Veterinary Microbiology and Immunology, Ontario Veterinary College, University of
Guelph, Guelph, Ontario NIG 2W1.
CAN. VET. JOUR., vol. 18, no. 10, October, 1977
and milk) and the health of the owners and of their family. The remaining 201 serum samples were obtained from female goats through the courtesy of Agriculture Canada. These samples had been submitted for brucellosis testing to the Federal Animal Pathology Laboratory, Guelph. No information, apart from their age, was available concerning these animals.
Testing procedure Serum samples were frozen at -20°C immediately upon receipt. They were inactivated by incubation at 56°C for 45 minutes immediately prior to testing. The Sabin-Feldman dye test was conducted in a standard manner using human accessory factor (9) and all goat sera were tested at a dilution of 1:16. The samples obtained from the selected farms were also titrated using fourfold dilutions to a final dilution of 1:1024. RESULTS
Of the 399 goat sera tested, 252 (63.1%) gave a positive reaction at a dilution of 1:16 or greater. In the samples obtained from selected farms, 55% of animals tested were positive while in those samples submitted for Brucella serology 71.1% were positive. This difference may be explained on the basis of the different age distributions within each sample population. For example, very few of the samples submitted for Brucella serology were from goats less than one year of age. As might be anticipated the prevalence of positive reactions varied with the age of the goat population (Figure 1). For example, of goats less than one year of age, 38/66 (57%) were seropositive, this dropped to 42% (28/67) of one year old animals, but thereafter climbed progressively to reach 85% (42/49) in four year old animals. The drop in prevalence during the first year of life may be a reflection of a loss of maternal immunity. A similar phenomenon is observed in humans (11). Because of the influence of age all further analyses were first adjusted to account for any differences in the age distribution of sample populations. There were no differences in the prevalence ,74
TOXOPLASMOSIS 0
100
o
.
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60
~60
38
50 40 30 20 10 0
c
766
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7,z
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ci
,I
5
FIGURE 1. The distribution of positive serological reactions to Toxoplasma gondii as a function of the age of goats. The fractions indicate the number of positive animals out of the number tested.
of positive reactions between the sexes. Thus male goats were 51.4% positive while female goats were 51.2% positive. When the samples taken from selected farms were investigated, the only factor which appeared to exert any direct influence on the percentage of positive reactions was the age distribution of the population sampled. No significant relationships emerged between the prevalence of positive reactions, the size of the goat herd, the major goat breed kept, the number of cats on the farm (most farms had cats), a history of abortions or stillbirths, or the occurrence of caseous lymphadenitis (Table I). No significant association was established between toxoplasmosis in goats and illness in humans although interestingly, the husband of one goat owner, was hospitalized with a suspected toxoplasma myocarditis during the course of this study. The distribution of antibody titers within the selected population (Figure 2) showed no unusual features and, unlike the distribution of titers within the human population was not biomodal (10). DISCUSSION These results are of interest from several
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Firstly, because the prevalence of positive reactions to Toxoplasma found in goats aspects.
0>.0
275
.x
CANADIAN VETERINARY JOURNAL ern Ontario and found nine
(52.9%) to be positive for toxoplasmosis (6). 60 The growing market for "natural foods" has * Humans led to an increasing demand for unpasteurized & 50 goat's milk for human consumption. In addi= 40 tion, the relatively small volumes of milk produced and the small number of farms in0 30 volved have combined to make it difficult for It 20 producers to get their milk pasteurized. For these reasons, it became apparent while ques10 tioning goat owners that a high proportion of the milk produced by dairy goats is consumed 0 or the owner's friends. Unfor'YJ6 1A6 1/64 1/256 2i1024 by the owner is it well tunately, recognized that unpasteurTiter ized goat's milk may serve as a source of FIGURE 2. The distribution of antibody titers Toxoplasma infection for humans (7). It is in 175 goats from selected farms compared with therefore not unlikely that the consumption the distribution observed in humans in southern of unpasteurized goat's milk may represent a Ontario. Human data derived from Reference 10. significant public health hazard. Goat meat in contrast, because of its "relatively strong flavor", appears to be generally well cooked is considerably higher than that seen in most in this country and if this is indeed the case, other species of domestic animal in southern then it is unlikely to represent a significant Ontario, secondly, because of a growing ten- source of infection. dency to consume unpasteurized goat's milk in Finally, in spite of the high prevalence of the interests of "health", and finally, because antibodies to this organism reported here we it is apparent that the occurrence of positive have not found it to be a significant clinical serological reactions in goats is not inevitably problem in goats. For this reason we would associated with severe clinical problems. disagree with the comments on this condition Unpublished data indicate that the preva- in Blood and Henderson (1). We consider lence of positive serological reactions to T. the disease to be enzootic in these animals in gondii among the domestic animals of south- this region and that any attempt to eradicate ern Ontario varies from 9% in horses, and 16% or even reduce the prevalence of this infection in cattle to 44% in swine and 65% in sheep. It by slaughter would be futile, at least until the is apparent therefore that sheep and goats precise source of infection of these animals may become infected much more frequently can be ascertained. than the other animals. The reasons for this are not clear. Our current understanding of SUMMARY the epidemiology of toxoplasmosis would suggest that herbivores acquire infection through With the Sabin-Feldman dye test, 252 out feline oocysts shed on grass (3). However, of 399 goat sera gave positive reactions for goats tend to browse rather than graze and antibodies to Toxoplasma gondii. This result while they are capable of cropping grass very is of significance from the public health aspect close to the ground, they will only do so if no particularly in view of the increasing conother food is available (8). They are also sumption of raw goat's milk and it is also of somewhat fastidious eaters and are therefore considerable epidemiological interest. unlikely to knowingly consume feline fecal material or dead mice. In view of this we RESUME' believe it possible that transmission of Toxoplasma to these animals might be by a comL'utilisation de l'epreuve au bleu de mepletely different and so far unidentified route. thylene de Sabin-Feldman a permis de deceler Toxoplasmosis also appears to be highly prev- des anticorps contre Toxoplasma gondii, dans alent in goats in other parts of the world. 252 des 399 echantillons de serum caprin Thus in Egypt 47% of goats are positive (5), eprouves a cette fin. Ce resultat s'avere signiand in Turkey 52% (13). In the U.S.A. the ficatif en ce qui concerne la sante publique, prevalence varies, it has been reported to be surtout si l'on tient compte de l'accroissement 43% (28/65) (2) in central New York and to actuel de la consommation de lait cru de be 27% (21/77) in northern California (12). chevre; il revet aussi un interet epidemioQuinn and McCraw tested 17 goats in south- logique considerable. 70
aI
Goats
FL1n .Fh
276
TOXOPLASMOSIS
7. RIEMNANN, H. P., M. E. MEYER, J. H. THEIS, G. KELSO and D. E. BEHYMIER. Toxoplasmosis in an infant fed unpasteurized goat's milk. J. Pediatrics 87: 573-576. 1975. 8. SABIN, A. B. Toxoplasmosis: Current status and unresolved problems. Introductory remarks. Am. J. trop. Med. Hyg. 2: 360-364. 1953. 9. SABIN, A. B. and H. A. FELDMAN. Dyes as microchemical indicators of a new immunity phenomenon affecting a protozoan parasite (Toxoplasma). Science 108: 660663. 1948. 10. TIZARD, I. R., S. S. CHAUHAN and C. H. LAI. The prevalence and epidemiology of toxoplasmosis in Ontario. J. Hyg., Camb. 78: 275-282. 1977. 11. TIZARD, I. R., P. J. QUINN and N. A. FISH. Some observations on the epidemiology of toxoplasmosis in Canada. J. Hyg., Camb. 77: 11-21. 1976. 12. VANDERWAGEN, L. C., D. E. BEHYMER, H. P. RIEMANN and C. E. FRANTI. A survey for Toxoplasma antibodies in northern California livestock and dogs. J. Am. vet. med. Ass. 164: 1034-1037. 1974. 13. WEILAND, G. and W. DALCHOW. Toxoplasma-Infektionen bei Haustieren in der Turkei. Berl. Munch. tierarztl. Wschr. 83: 6568. 1970.
ACKNOWLEDGNIENTS
This work was supported by the Ontario Ministry of Health. REFERENCES 1. BLOOD, D. C. and J. A. HENDERSON. Veterinary Medicine, 4th Edition. London: Balliere, Tindall. 1974. 2. FELDMAN, H. A. and L. T. MILLER. Sero-
logical study of toxoplasmosis prevalence. Am. J. Hyg. 64: 320-335. 1956. 3. FRENKEL, J. K. Toxoplasmosis. In Parasite Life Cycle, Pathology, and Immunology in the Coccidia. D. M. Hammond and P. L. Long, Editors. Baltimore: University Park Press. 1973. 4. HAFEZ, E. S. E. and J. P. SCOTT. The behaviour of sheep and goats. In The Behaviour of Domestic Animals. E. S. E. Hafe7, Editor. London: Balliere, Tindall, and Cox. 1962. 5. MARONPOT, R. R. and B. A. M. BOTROS. Toxoplasma serologic survey on man and domestic animals in Egypt. J. Egypt. publ. Hlth Ass. 47: 58-67. 1972.
6. QUINN, P. J. and B. M. MCCRAW. Current status of Toxoplasma and toxoplasmosis. A review. Can. vet. J. 13: 247-262. 1972.
SCHERING AWARD FOR VETERINARY STUDENTS Schering awards are offered to senior students in each of the three Canadian Veterinary Colleges. Three $100 awards will be available to each college.
3. 4.
RULES 1. Eligibility. The competition is limited to students in their final year at a Canadian veterinary college. 2. The awards will be given for the best case reports, preferably of 300-1,000 words, written in a form acceptable for publication in the Canadian Veterinary Journal.
277
5.
6.
Please consult "Instructions to Authors" and recent issues of the Journal for form. Entries will be accepted in either English or French. A committee from each College will be responsible for selecting the ten best case reports which will be judged by the Editorial Board of the Canadian Veterinary Medical Association. The awards will be presented at a suitable function. The Journal reserves the right to publish the prize-winning papers subject to the usual editorial procedures.
