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The prevalence of Toxoplasma gondii antibodies in man in Plateau State and meat animals in Nigeria
TRANSACTIONS OFTHEROYALSOCIETY OFTROPEAL MEDKINEANDHYGIENE (1985)79, 21-23
The prevalence
21
of Toxoplasma gondii antibodies in man in Plateau State and meat animals in Nigeria
T. I. 0. OSIYEMI, ELIZABETH M. M. SYNGE*, D. E. AGBONLAHOR AND ROSE AGBAVWE National Veterinary Research Institute, Vom, Nigeria Absdact
Toxoplasmagondii antibodies were found in the sera of 22.86% of people in the Jos area of Plateau State, Nigeria. The incidence of antibodies in Nigerian food animals was 1740%, the highest being in sheep (21.92%) and lowest in goats (13.88%). Cattle and horseswere roughly equally infected-about 17*0%. The zoonotic potential of T. a&ii in food animals is stressedand epidemiological factors are reviewed. Introduction
Toxoplasma gondii infection is an aberrant feline coccidial disease occurring also in other vertebrates (OSIYEMI, 1976). Toxoplasmosis has been shown to be distributed world-wide (JACOBS, 1957; BEATTIE, 1959). Human caseshave been reported in Nigeria by JELLIFFE (1951) and MIDDLEMISS (1957). More recently serological evidence of the diseasein man and livestock in Nigeria has been published (LUDLAM, 1965; OLIJRIN et al., 1972; FALADE, 1978; OGUNBA & THOMAS, 1979; MAIUNDE
& EZEH, 1981). The
epidemiological importance of the diseasein Nigerian livestock has been relatively little studied. However, it is important to know the possible sourcesof human infection from food animals. Such an observation may shed some light on sources of congenital transmission in man (KAIuhi & LUDLAM, 1975). This paper presents additional serological evidence of toxoplasmosis in man and livestock in Nigeria. Materials aod Methods 2 10 human sera were obtained for examination. 99 of them
were from Murtala Hospital in Jos; 69 were sera from women attending ante-natal clinics (aged 14 to 46 years) and 30 were from men (aged 25 to 70 years) with a history of pyrexia of unknown origin. The mmaining 111 sera were from persons of unknown medical history (but aged between three months and 70 years) collected from Vom General Hospital and from the School of Medical Laboratory Technology, Vom. 300 sera from cattle, 34 from goats, 90 from horsesand 114 from sheep were examined. Their origins are shown in Table II. All the sera were stored at -20°C until tested. Before use all sera were inactivated at 56°C for 30 min. The other reagents were obtained from Wellcome Reagents Limited, England. These were: (a) test cells (antigen&a 2.25% suspension of formalinixed tanned turkey red blood cells sensitized with a soluble sonicate of T. g&G’:2 control cells-a 2.25% suspension of formahmmd turkey red blood cells; (c) diluent buffer which was phosphate buffered saline pH 7.2 containing 1.5% normal rabbit serum and 0.1% sodium axide; (d) positive control serum-sheep serum containing 0.1% sodium axide. The positive control serum gives a positive screening test and reacts to a dilution between 1:256 and 1:1024 in the quantitative test; (e) negative control-bovine serum containing 0.1% sodium axide. The negative control serum does not causeagglutination of test or control cells at any dilution in the test described. The test procedure used followed the recommendation in Wellcome ToxHatest Haemagglutination Kit which was
based upon indirect haemagglutination test, IHAT, for toxoplasmosis according to JACOBS 81LUND (1957), modified by other workers (THORBURN& WILLIAMS, 1972; JENNIS, 1966; KARIM & LUDLAM, 1975a).The tests were carried out in micro&e plates, V wells obtained from Dynatech Laboratories Limited, Daux Road, Billingshurst, England. All the inactivated set-awere screenedat l/64 serum dilution. Positive samples at that dilution were subsequently quantitated to obtain their toxoplasma antibody levels. The plates were read after 2.5 hours and the highest dilution of serum that gave an irregular rough button of red blood surrounded by a lawn covering the entire bottom of the well was taken as the end point. Results
Of the whole population tested 22.86% were positive (Table I). 26.7% of sera from the men, 18.84%from the women of 24.32% of the people from Vom tested had Toxoplasma antibodies. Table II shows the proportion of the food animals with Toxoplasma antibodies; sheep had the highest incidence rate of 21.92% followed by horses and cattle, 17.78 and 16*0%, respectively. Coats had the lowest incidence, 13.88%. Of the total number of food animals 17.4% had Toxoplasma antibodies. Table I-Showing Area of Plateau
tbe proportion of tested people in Jos State with humoral antibodies against Toxoplasmagundii determiaed by IHAT* No.
Sex
tested
Male Female Mixed**
111
Total
210
30 69
Source
Jos Jos
No.
%
+ve
+ve
8
26.70
13
18.84
Vom
27
24.32
Jos Area
48
22.86
*Positive titre is taken from l/256 and above. **Sera from both sexes-all of unknown history. Discussion
The results clearly indicate the incidence of T. gomfii infection in man and animals in areasof Nigeria in which they live. Several workers including FAIRCHILD et al. (1967), FRENKEL (1973) and KAFUM& LUDLAM (1975b), have shown that at the level of positive titre chosen, the IHAT is more sensitive than other serological tests in evaluating Toxoplasmainfec*Present Address: Waterheads, Peebles, Scotland, UK.
22 g+*lI-The Mean animals Cattle Goats Horses Sheep
T. gondii proportion
ANTIBODIES
IN
MAN
AND
ANIMALS
IN
NIGERIA
of food animals with humoral antibodies against Toxoplasma gondii determined
Source Mubi Jos Abattoir g”$+p
No. tested
No. +ve
% +ve 16.00 13.88 22.2 4.16 25.00 20.00 37.93 .) 15.09
Wildlife Park Jos Jos Abattoir Maiduguri Kane Kaduna Fulani Flock Vom
17.78
21.92
2Z.E
Total All 540 *Positive titre taken from l/256 and above. tion in man and animals in conditions where only single serum samples are available. JACOBSet al. (1960) and MUNDAY (1975) have shown that infected food animals, e.g., cattle, pigs and sheep are some of the sources of human Toxoplasma infection because Toxoplasma have been shown to survive in skeletal muscle (SCOTT, 1978). However, a parasitological survey of the diaphragmatic muscle of somecattle and sheep slaughtered at the Jos Municipal Abattoir yielded no isolation of T. go&i (Osiyemi, unpublished). The incidence figures in Table II on the infection rate in livestock indicate the extent of the occupational hazard in the abattoir and home kitchen, and also suggest that mutton is more infectious than other meat and that goat meat appearsto be lessdangerous. All the animals shown in Table II are sources of meat for human consumption in Nigeria. It is still not clear whether a higher incidence of Toxodusma antibodies is likelv to occur in oeoole with close; contact with infect&s toxoplasmas, e.g., cooks, butchers and women (who in Nigeria traditionally do most of the cooking) and in people who consume a lot of roasted meat, locally called ‘Suya’, which might contain dangerous toxoplasmas. Higher rates of infections can also occur in both man and animals as a result of environmental contamination by mature oocysts from infected Felidae, wild or domestic, which provide for widespread distribution of Toxoplasma oocysts in nature (RUIZ et al., 1973). Previous investigations by GIBSON & COLEMAN (1958) and FULTONet al. (1966) showed that climatic factors such as rainfall and temperature, and the closeness of association with wild and domestic animals, may influence the proportion of the population affected; warm wet areashave higher prevalence rates than dry high areas. This observation was confirmed for towns in Rivers state (Niger Delta) and in Oyo State (Ibadan) by LUDLAM (1965) and OGUNBA& THOMAS(1979) where the incidence rates vary from 64.5% to 20.6% in normal people. The same is true for the Ibadan and Jos areas of Plateau State with similar annual rainfall (BUCHANAN & PUGH, 1%9), Toxoplasma antibody incidence being 20.6% and 22*2%, respectively. It is consistently found that the antibody titres in most Nigerians with
by
94
1740
some underlying pathological processes are much higher than in normal Nigerians (OLURIN et al., 1972; OGUNBA& THOMAS, 1979). FALADE (1978) found 27 of 848 goats (3.2%) in Ibadan positive. MAKINDE & EZEH (1981) found 37 of 638 Nigerian cattle (5.8%) positive for infection, but the climatic conditions of the sources are unknown. The result of investigations of livestock now presented indicate variations between different geographical areas within the country (Table II). In domestic animal!, the rate of infection, among other factors, may be mtluenced by species susceptibility, closeness of grazing habit and the availability of numerous viable oocysts from feral Felidae with coccidial infections. In Nigeria, regional differences in the levels of Toxo&sma antibodies in man and animals can be expected from these epidemiological factors which govern infection. These include occupational hazards, dietary predispositions, density of feral and domestic felidae, and climatic conditions which facilitate the development of oocysts available for natural challenge. Undoubtedly in Nigeria these factors will vary from place to place. Acknowledgements
We wish to thank Prof. E. 0. Ogunbaof the Collegeof Medicine,University of Ibadanand Dr. R. A. Joshuaof the Nigerian Institute for TrypanosomiasisResearchfor their criticism and Dr. A. G. Lamorde, Director, National Veterinary ResearchInstitute, Vom, for permission fo publish. References
Beattie, C. P. (1959).Discussionon Toxoplasmosis.Pro-
ceedings of the Royal Society of Medicine, 53, 108-111. Buch++ K. M. & Pug!, J. .C. (1969). Land ana’ People in y’,ea. London: Umversnyof London PressLtd., pp.
-. -<. Falade,S. (1978).Toxopkzsma gondii antibodiesin Nigeria goats.Tropical Animal Health and Product&m, 10, 175 177.
Fairchild, G. A., Greenwald,P. & Decker,H. A. (1967). An evaluation of the indirect haemagglutinationtest for Toxoplasmosis.American journal of Tropical Medicine and Hygiene, 16, 278-283.
T.
I.
0.
OSIYEhiI
Frenkel, J. K. (1973). Toxoplasmosis: parasite life cycle, pathology and immunology. In: The Coccidiu. Hammond, D. M. & Long, P. L. (Editors). London: Buttenvorth, pp. 343-410. F&on, J. D., Fleck, D. G. & Payne, R. A. (1966). Prevalence of Toxoplasma antibodies in sera from Greece and Africa. Joumal of Hygiene, 64, 75-79. Gibson, C. L. & Coleman, N. (1958). The prevalence of Toxoplasma antibodies in Guatar@a and Costa Rica. t34
Joumal
of Tropical Medume and Hygiene, I,
Jacobs., L. ‘( 1957). The interrelation of toxoplasmosis in swme? cattle, dogs and man. Public Health Reports, Washmgton, 72, 872-882.
Jacobs, L., Remington, J. S. & Melton, M. L. (1960). A survey of meat samples for swine, cattle, and sheep for the presence of encysted Toxoplasma. Journal of Parasiwlogy, 46, 23-28. Jacobs, L. & Lund:, 111.N. (1957). Haemagglutination test for toxoplasmosis. Science, 125, 1035. Jell&, D. B. (1951). Congenital toxoplasmosis in African child. Archives of LXseases in Childhood, 2$, 258-260. Jemtis, P. (1966). A simpli6ed haemagglutinauon test for toxoplasmosis using p.ic aldehyde treated cells. Australum Joumal
of
qmmental
Bwlogy and Medrcal
Science, 44, 317-322. Karim, K. A. & Ludlam, G. B. (1975a). The relationship and signiticance of antibody titres as determined by various serological methods in glandular and ocular toxoplasmosis. Journal of Clinical Pathology, 28, 42-49. Karim, K. A. & Ludlam, G. B. (1975b). Serological diagnosis of congenital toxoplasmosis.Journal of Clinical Pathology,
28, 383-387.
et
23
al.
Ludlam, G. B. (1%5). Toxoplasma antibodies in the inhabitants of the Niger Delta. Transactions of the Royal Society of Tropical Medicine and Hygiene, SO, 83-86.
Makinde, A. A. & Ezeh, A. 0. (1981). Serological survey of Toxopkmna gundii m Nigerian cattle. A prehminary report. British Veminary Journal, 137, 485-488. Middlemiss, J. H. (1957). Discussion at the meeting of 17 January 1957. Transactions of Royal Socie~ of Tropical Medicine and Hygiene, 51, 122. Munday, B. L. (1975). Prevalence of toxoplasmosis in Tasmanian mean animals. Australian Veterinary 3owna1, 51, 315-316. Ohirin, O., Fleck, D. G. & Osuntokun, B. (1972). Toxo lasmosis and chorioretinitis in Nigeria. Tropical and &qraphical
Medicine, 24, 240-245.
Ogunba, E. 0. & Thomas, V. (1979). Antibodies to Toxo@asma gondii in Ibadan. Nigerian3oumal of Medical Sciences,
2, 77-80.
Osiyemi, T. I. 0. (1976). A comparison o mod
used in ovine wzco&smosis. M.Sc. =i--hesis~~:~ university.
Ruix, A., Frenkel, J. K. & Cerdas, L. (1973). Isolation of Toxoplasma from soil. 3oumal of Parasitology, 59, 204. Scott, R. J. (1978). Toxoplasmosis. Tropical Diseases Bulle-
fin, 75, 809.827.
Thorburn, H. & Williams, H. (1972). A stable haemagglutitrating antigen for detecting toxoplasma antibodies. Journal of Clinical Pathology, 25, 762-767.
Acceptedfor publication 13th September,1983 (delayed by
loss
in
mail).
The prevalence
21
of Toxoplasma gondii antibodies in man in Plateau State and meat animals in Nigeria
T. I. 0. OSIYEMI, ELIZABETH M. M. SYNGE*, D. E. AGBONLAHOR AND ROSE AGBAVWE National Veterinary Research Institute, Vom, Nigeria Absdact
Toxoplasmagondii antibodies were found in the sera of 22.86% of people in the Jos area of Plateau State, Nigeria. The incidence of antibodies in Nigerian food animals was 1740%, the highest being in sheep (21.92%) and lowest in goats (13.88%). Cattle and horseswere roughly equally infected-about 17*0%. The zoonotic potential of T. a&ii in food animals is stressedand epidemiological factors are reviewed. Introduction
Toxoplasma gondii infection is an aberrant feline coccidial disease occurring also in other vertebrates (OSIYEMI, 1976). Toxoplasmosis has been shown to be distributed world-wide (JACOBS, 1957; BEATTIE, 1959). Human caseshave been reported in Nigeria by JELLIFFE (1951) and MIDDLEMISS (1957). More recently serological evidence of the diseasein man and livestock in Nigeria has been published (LUDLAM, 1965; OLIJRIN et al., 1972; FALADE, 1978; OGUNBA & THOMAS, 1979; MAIUNDE
& EZEH, 1981). The
epidemiological importance of the diseasein Nigerian livestock has been relatively little studied. However, it is important to know the possible sourcesof human infection from food animals. Such an observation may shed some light on sources of congenital transmission in man (KAIuhi & LUDLAM, 1975). This paper presents additional serological evidence of toxoplasmosis in man and livestock in Nigeria. Materials aod Methods 2 10 human sera were obtained for examination. 99 of them
were from Murtala Hospital in Jos; 69 were sera from women attending ante-natal clinics (aged 14 to 46 years) and 30 were from men (aged 25 to 70 years) with a history of pyrexia of unknown origin. The mmaining 111 sera were from persons of unknown medical history (but aged between three months and 70 years) collected from Vom General Hospital and from the School of Medical Laboratory Technology, Vom. 300 sera from cattle, 34 from goats, 90 from horsesand 114 from sheep were examined. Their origins are shown in Table II. All the sera were stored at -20°C until tested. Before use all sera were inactivated at 56°C for 30 min. The other reagents were obtained from Wellcome Reagents Limited, England. These were: (a) test cells (antigen&a 2.25% suspension of formalinixed tanned turkey red blood cells sensitized with a soluble sonicate of T. g&G’:2 control cells-a 2.25% suspension of formahmmd turkey red blood cells; (c) diluent buffer which was phosphate buffered saline pH 7.2 containing 1.5% normal rabbit serum and 0.1% sodium axide; (d) positive control serum-sheep serum containing 0.1% sodium axide. The positive control serum gives a positive screening test and reacts to a dilution between 1:256 and 1:1024 in the quantitative test; (e) negative control-bovine serum containing 0.1% sodium axide. The negative control serum does not causeagglutination of test or control cells at any dilution in the test described. The test procedure used followed the recommendation in Wellcome ToxHatest Haemagglutination Kit which was
based upon indirect haemagglutination test, IHAT, for toxoplasmosis according to JACOBS 81LUND (1957), modified by other workers (THORBURN& WILLIAMS, 1972; JENNIS, 1966; KARIM & LUDLAM, 1975a).The tests were carried out in micro&e plates, V wells obtained from Dynatech Laboratories Limited, Daux Road, Billingshurst, England. All the inactivated set-awere screenedat l/64 serum dilution. Positive samples at that dilution were subsequently quantitated to obtain their toxoplasma antibody levels. The plates were read after 2.5 hours and the highest dilution of serum that gave an irregular rough button of red blood surrounded by a lawn covering the entire bottom of the well was taken as the end point. Results
Of the whole population tested 22.86% were positive (Table I). 26.7% of sera from the men, 18.84%from the women of 24.32% of the people from Vom tested had Toxoplasma antibodies. Table II shows the proportion of the food animals with Toxoplasma antibodies; sheep had the highest incidence rate of 21.92% followed by horses and cattle, 17.78 and 16*0%, respectively. Coats had the lowest incidence, 13.88%. Of the total number of food animals 17.4% had Toxoplasma antibodies. Table I-Showing Area of Plateau
tbe proportion of tested people in Jos State with humoral antibodies against Toxoplasmagundii determiaed by IHAT* No.
Sex
tested
Male Female Mixed**
111
Total
210
30 69
Source
Jos Jos
No.
%
+ve
+ve
8
26.70
13
18.84
Vom
27
24.32
Jos Area
48
22.86
*Positive titre is taken from l/256 and above. **Sera from both sexes-all of unknown history. Discussion
The results clearly indicate the incidence of T. gomfii infection in man and animals in areasof Nigeria in which they live. Several workers including FAIRCHILD et al. (1967), FRENKEL (1973) and KAFUM& LUDLAM (1975b), have shown that at the level of positive titre chosen, the IHAT is more sensitive than other serological tests in evaluating Toxoplasmainfec*Present Address: Waterheads, Peebles, Scotland, UK.
22 g+*lI-The Mean animals Cattle Goats Horses Sheep
T. gondii proportion
ANTIBODIES
IN
MAN
AND
ANIMALS
IN
NIGERIA
of food animals with humoral antibodies against Toxoplasma gondii determined
Source Mubi Jos Abattoir g”$+p
No. tested
No. +ve
% +ve 16.00 13.88 22.2 4.16 25.00 20.00 37.93 .) 15.09
Wildlife Park Jos Jos Abattoir Maiduguri Kane Kaduna Fulani Flock Vom
17.78
21.92
2Z.E
Total All 540 *Positive titre taken from l/256 and above. tion in man and animals in conditions where only single serum samples are available. JACOBSet al. (1960) and MUNDAY (1975) have shown that infected food animals, e.g., cattle, pigs and sheep are some of the sources of human Toxoplasma infection because Toxoplasma have been shown to survive in skeletal muscle (SCOTT, 1978). However, a parasitological survey of the diaphragmatic muscle of somecattle and sheep slaughtered at the Jos Municipal Abattoir yielded no isolation of T. go&i (Osiyemi, unpublished). The incidence figures in Table II on the infection rate in livestock indicate the extent of the occupational hazard in the abattoir and home kitchen, and also suggest that mutton is more infectious than other meat and that goat meat appearsto be lessdangerous. All the animals shown in Table II are sources of meat for human consumption in Nigeria. It is still not clear whether a higher incidence of Toxodusma antibodies is likelv to occur in oeoole with close; contact with infect&s toxoplasmas, e.g., cooks, butchers and women (who in Nigeria traditionally do most of the cooking) and in people who consume a lot of roasted meat, locally called ‘Suya’, which might contain dangerous toxoplasmas. Higher rates of infections can also occur in both man and animals as a result of environmental contamination by mature oocysts from infected Felidae, wild or domestic, which provide for widespread distribution of Toxoplasma oocysts in nature (RUIZ et al., 1973). Previous investigations by GIBSON & COLEMAN (1958) and FULTONet al. (1966) showed that climatic factors such as rainfall and temperature, and the closeness of association with wild and domestic animals, may influence the proportion of the population affected; warm wet areashave higher prevalence rates than dry high areas. This observation was confirmed for towns in Rivers state (Niger Delta) and in Oyo State (Ibadan) by LUDLAM (1965) and OGUNBA& THOMAS(1979) where the incidence rates vary from 64.5% to 20.6% in normal people. The same is true for the Ibadan and Jos areas of Plateau State with similar annual rainfall (BUCHANAN & PUGH, 1%9), Toxoplasma antibody incidence being 20.6% and 22*2%, respectively. It is consistently found that the antibody titres in most Nigerians with
by
94
1740
some underlying pathological processes are much higher than in normal Nigerians (OLURIN et al., 1972; OGUNBA& THOMAS, 1979). FALADE (1978) found 27 of 848 goats (3.2%) in Ibadan positive. MAKINDE & EZEH (1981) found 37 of 638 Nigerian cattle (5.8%) positive for infection, but the climatic conditions of the sources are unknown. The result of investigations of livestock now presented indicate variations between different geographical areas within the country (Table II). In domestic animal!, the rate of infection, among other factors, may be mtluenced by species susceptibility, closeness of grazing habit and the availability of numerous viable oocysts from feral Felidae with coccidial infections. In Nigeria, regional differences in the levels of Toxo&sma antibodies in man and animals can be expected from these epidemiological factors which govern infection. These include occupational hazards, dietary predispositions, density of feral and domestic felidae, and climatic conditions which facilitate the development of oocysts available for natural challenge. Undoubtedly in Nigeria these factors will vary from place to place. Acknowledgements
We wish to thank Prof. E. 0. Ogunbaof the Collegeof Medicine,University of Ibadanand Dr. R. A. Joshuaof the Nigerian Institute for TrypanosomiasisResearchfor their criticism and Dr. A. G. Lamorde, Director, National Veterinary ResearchInstitute, Vom, for permission fo publish. References
Beattie, C. P. (1959).Discussionon Toxoplasmosis.Pro-
ceedings of the Royal Society of Medicine, 53, 108-111. Buch++ K. M. & Pug!, J. .C. (1969). Land ana’ People in y’,ea. London: Umversnyof London PressLtd., pp.
-. -<. Falade,S. (1978).Toxopkzsma gondii antibodiesin Nigeria goats.Tropical Animal Health and Product&m, 10, 175 177.
Fairchild, G. A., Greenwald,P. & Decker,H. A. (1967). An evaluation of the indirect haemagglutinationtest for Toxoplasmosis.American journal of Tropical Medicine and Hygiene, 16, 278-283.
T.
I.
0.
OSIYEhiI
Frenkel, J. K. (1973). Toxoplasmosis: parasite life cycle, pathology and immunology. In: The Coccidiu. Hammond, D. M. & Long, P. L. (Editors). London: Buttenvorth, pp. 343-410. F&on, J. D., Fleck, D. G. & Payne, R. A. (1966). Prevalence of Toxoplasma antibodies in sera from Greece and Africa. Joumal of Hygiene, 64, 75-79. Gibson, C. L. & Coleman, N. (1958). The prevalence of Toxoplasma antibodies in Guatar@a and Costa Rica. t34
Joumal
of Tropical Medume and Hygiene, I,
Jacobs., L. ‘( 1957). The interrelation of toxoplasmosis in swme? cattle, dogs and man. Public Health Reports, Washmgton, 72, 872-882.
Jacobs, L., Remington, J. S. & Melton, M. L. (1960). A survey of meat samples for swine, cattle, and sheep for the presence of encysted Toxoplasma. Journal of Parasiwlogy, 46, 23-28. Jacobs, L. & Lund:, 111.N. (1957). Haemagglutination test for toxoplasmosis. Science, 125, 1035. Jell&, D. B. (1951). Congenital toxoplasmosis in African child. Archives of LXseases in Childhood, 2$, 258-260. Jemtis, P. (1966). A simpli6ed haemagglutinauon test for toxoplasmosis using p.ic aldehyde treated cells. Australum Joumal
of
qmmental
Bwlogy and Medrcal
Science, 44, 317-322. Karim, K. A. & Ludlam, G. B. (1975a). The relationship and signiticance of antibody titres as determined by various serological methods in glandular and ocular toxoplasmosis. Journal of Clinical Pathology, 28, 42-49. Karim, K. A. & Ludlam, G. B. (1975b). Serological diagnosis of congenital toxoplasmosis.Journal of Clinical Pathology,
28, 383-387.
et
23
al.
Ludlam, G. B. (1%5). Toxoplasma antibodies in the inhabitants of the Niger Delta. Transactions of the Royal Society of Tropical Medicine and Hygiene, SO, 83-86.
Makinde, A. A. & Ezeh, A. 0. (1981). Serological survey of Toxopkmna gundii m Nigerian cattle. A prehminary report. British Veminary Journal, 137, 485-488. Middlemiss, J. H. (1957). Discussion at the meeting of 17 January 1957. Transactions of Royal Socie~ of Tropical Medicine and Hygiene, 51, 122. Munday, B. L. (1975). Prevalence of toxoplasmosis in Tasmanian mean animals. Australian Veterinary 3owna1, 51, 315-316. Ohirin, O., Fleck, D. G. & Osuntokun, B. (1972). Toxo lasmosis and chorioretinitis in Nigeria. Tropical and &qraphical
Medicine, 24, 240-245.
Ogunba, E. 0. & Thomas, V. (1979). Antibodies to Toxo@asma gondii in Ibadan. Nigerian3oumal of Medical Sciences,
2, 77-80.
Osiyemi, T. I. 0. (1976). A comparison o mod
used in ovine wzco&smosis. M.Sc. =i--hesis~~:~ university.
Ruix, A., Frenkel, J. K. & Cerdas, L. (1973). Isolation of Toxoplasma from soil. 3oumal of Parasitology, 59, 204. Scott, R. J. (1978). Toxoplasmosis. Tropical Diseases Bulle-
fin, 75, 809.827.
Thorburn, H. & Williams, H. (1972). A stable haemagglutitrating antigen for detecting toxoplasma antibodies. Journal of Clinical Pathology, 25, 762-767.
Acceptedfor publication 13th September,1983 (delayed by
loss
in
mail).