Seroprevalence of toxoplasmosis in sheep in South Africa.

Abstract

Serum samples from 600 sheep were collected from 5 different provinces randomly chosen in South Africa. Two sheep abattoirs (representing formal slaughter of sheep) and 1 rural location (representing informal slaughter of sheep) per province were also selected randomly. The serum samples were tested for anti-Toxoplasma gondii IgG antibodies using 2 different serological tests: an indirect fluorescent antibody (IFA) test and an enzyme-linked immunosorbent assay (ELISA) test available as a commercial kit. This study provides the first published data on seroprevalence of toxoplasmosis in sheep in South Africa, although positive titres have been found previously in wild felids, ferrets, chinchillas and a dog. Data on seroprevalence in sheep is considered important because consumption of mutton is universally considered to be a source of zoonotic transfer to humans. Seroprevalence in humans in South Africa was previously found to be 20 % and it is postulated that this may be linked to the informal slaughter and consumption of mutton. During this study, the overall national seroprevalence per province in sheep was found to be 5.6 % (IFA) and 4.3 % (ELISA), respectively. This is lower than in other countries, possibly because South Africa has an arid climate. Differences in seroprevalence in different areas studied suggested an association with the climate and a significant correlation (P > 0.05) was detected between the prevalence of T. gondii and the minimum average temperature. The seroprevalence was found to be significantly higher (P < 0.01) in sheep originating from commercial farms (7.9 %) than in rural sheep in the informal sector (3.4 %). Also, sheep managed extensively had a seroprevalence of 1.8 %, which was significantly lower (P < 0.05) than the seroprevalence in sheep under semi-intensive or intensive management systems (5.3%). An incidental finding of interest was the considerable movement of sheep to abattoirs and mutton after slaughter. The highest consumption of mutton was in the Western Cape Province (29.9%) while the highest concentration of sheep is found in the Eastern Cape Province (30.1%).

Full text

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1160038-2809 Tydskr.S.Afr.vet.Ver. (2007) 78(3): 116–120
Article — Artikel
Seroprevalence of toxoplasmosis in sheep in South Africa
N Abu Samra
a, C M E McCrindle
a*, B L Penzhorn
band B Cenci-Goga
c
INTRODUCTION
Toxoplasma gondii is an intracellular
protozoan with a large number of inter-
mediate hosts, including all warm-
blooded animals (mammals and birds)
and humans, and felids are its definitive
hosts5. Serological surveys have been
done in various parts of the world and
showthatmorethanathirdofthehuman
population have antibodies against
T. gondii. This high seroprevalence in
humans demonstrates its importance as
a zoonotic disease. This has even more
relevance now than when most sero-
prevalence studies were originally
carried out, because of the current high
risk of toxoplasmosis for HIV positive
people5. Ingestion of undercooked mut-
ton is regarded as an important source of
infection for toxoplasmosis in humans16.
In South Africa a human seroprevalence
of20%wasdetectedin1978byJacobsand
Manson8.
Despitethefactthatthereissomelitera-
ture on the seroprevalence of toxo-
plasmosis in wild felids, chinchillas,
ferrets, free-ranging wild felids, cheetah
and a dog1,3,4,12,20,21, there were no data on
the seroprevalence in sheep in South
Africa, although these data are available
for many other countries2,6,7,11,14,16,18,22. Data
on seroprevalence in sheep are consid-
ered important because consumption of
mutton is universally considered to be a
source of zoonotic transfer to humans16.
Theestimatedworldwideseroprevalence
oftoxoplasmosisinlivestockis;cattle9%,
sheep30%andgoats15%5.Althoughthe
infection in animals is often asymptom-
atic, abortion storms in sheep have also
been decribed worldwide6.
Sheep farming, for both wool and mut-
ton, occupies approximately 590 000 km2
of South Africa, which represents 53 % of
allagriculturalland10.TheprevalenceofT.
gondii in humans in South Africa is likely
toberelatedtotheprevalenceofseroposi-
tivecasesinsheepasitiselsewhereinthe
world16. The actual distribution of
toxoplasmosis in sheep in South Africa
was not known, but it was important to
study the situation, because of the high
consumption of mutton in this country10.
The aim of this study was to investigate
the seroprevalence of T. gondii in sheep in
South Africa.
MATERIALS AND METHODS
Five of the 8 provinces of South Africa
were chosen randomly to undertake this
study17. The provinces were KwaZulu-
Natal, Eastern Cape, Western Cape,
Gauteng and Free State. A list of sheep
abattoirswasobtainedfromtheRedMeat
Abattoir Association. In every province 2
abattoirswererandomlyselectedforsam-
pling.Thesheepsampledatabattoirsrep-
resented the formal or commercial sector.
One state veterinary district was selected
perprovincefromalistobtainedfromthe
NationalDepartmentofAgriculture,soas
to sample animals belonging to
small-scale sheep farmers (representing
theinformalmarketingsector).Attheend
of the study, a total of 600 serum samples
was collected. Extra animals were sam-
pledtocompensateforproblemsencoun-
tered while transporting or handling the
sera.
The origins of the sampled sheep were
traced using records supplied by the
abattoir managers. Traceability com-
prised both backward tracing to the
location of the farm of origin as well as
forward tracing to the location of the
butchers that bought the carcasses for
retail distribution and sale to consum-
ers. It was presumed that most of the
sheep from the informal sector would be
aDepartment of Paraclinical Sciences, Faculty of Veteri-
nary Science, University of Pretoria, Private Bag X04,
Onderstepoort, 0110 South Africa.
bDepartment of Veterinary Tropical Diseases, Faculty of
Veterinary Science, University of Pretoria, Private Bag
X04, Onderstepoort, 0110 South Africa.
cDepartmento d’Ispezione degli Alimenti di origine Veteri-
naria, University of Perrugia, 01600 Perugia, Italy.
*Author for correspondence.
E-mail: cheryl.mccrindle@up.ac.za
Received: March 2007. Accepted: July 2007.
ABSTRACT
Serumsamplesfrom600sheepwerecollectedfrom5differentprovincesrandomlychosen
in South Africa. Two sheep abattoirs (representing formal slaughter of sheep) and 1 rural
location (representing informal slaughter of sheep) per province were also selected
randomly.Theserumsamplesweretestedforanti-ToxoplasmagondiiIgGantibodiesusing2
differentserologicaltests:anindirectfluorescentantibody(IFA)testandanenzyme-linked
immunosorbent assay (ELISA) test available as a commercial kit. This study provides the
first published data on seroprevalence of toxoplasmosis in sheep in South Africa, although
positivetitreshavebeenfoundpreviouslyinwildfelids,ferrets,chinchillasandadog.Data
on seroprevalence in sheep is considered important because consumption of mutton is
universally considered to be a source of zoonotic transfer to humans. Seroprevalence in
humans in South Africa was previously found to be 20 % and it is postulated that this may
be linked to the informal slaughter and consumption of mutton. During this study, the
overall national seroprevalence per province in sheep was found to be 5.6 % (IFA) and
4.3 % (ELISA), respectively. This is lower than in other countries, possibly because South
Africa has an arid climate. Differences in seroprevalence in different areas studied
suggested an association with the climate and a significant correlation (P > 0.05) was
detected between the prevalence of T. gondii and the minimum average temperature. The
seroprevalence was found to be significantly higher (P < 0.01) in sheep originating from
commercial farms (7.9 %) than in rural sheep in the informal sector (3.4 %). Also, sheep
managed extensively had a seroprevalence of 1.8 %, which was significantly lower (P <
0.05) than the seroprevalence in sheep under semi-intensive or intensive management
systems (5.3 %). An incidental finding of interest was the considerable movement of sheep
to abattoirs and mutton after slaughter. The highest consumption of mutton was in the
Western Cape Province (29.9 %) while the highest concentration of sheep is found in the
Eastern Cape Province (30.1 %).
Key words: seroprevalence, sheep, toxoplasmosis, veterinary public health.
Abu Samra N, McCrindle C M E, Penzhorn B L, Cenci-Goga B Seroprevalence of
toxoplasmosis in sheep in South Africa. Journal of the South African Veterinary Association
(2007) 78(3): 116–120 (En.). Department of Paraclinical Sciences, Faculty of Veterinary Sci-
ence, University of Pretoria, Private Bag X04, Onderstepoort, 0110 South Africa.

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0038-2809 Jl S.Afr.vet.Ass. (2007) 78(3): 116–120 117
slaughtered and consumed close to the
rural area where they were located.
Information on proportional mutton
consumption per province in South Africa
wasobtainedfromtheShoprite/Checkers
SupermarketChain(DDiemont,Division
Meat Markets, pers. comm., 2006).
Blood collection
Blood (c. 4 m ) was collected from the
jugular vein of sheep at abattoirs (prior to
slaughter) and on rural farms. The blood
samples were transported on ice to the
laboratory. After clotting, the samples
were centrifuged at 3000 g for 10 min and
the serum decanted. The serum speci-
menswerestoredat–20°Cbeforeanalysis
in the Serology Laboratory of the Depart-
ment of Tropical Disease, University of
Pretoria, Onderstepoort.
Serological analysis
Two serological tests were used for the
detection of antibodies to T. gondii: the
enzyme-linked immunosorbent assay
(ELISA) test and the indirect fluores-
cent antibody (IFA) test. The agreement
between the 2 tests was calculated by
using the kappa value, as κ = (OP–
EP/(1–EP)17.
FortheELISAtest,acommercialenzyme
immuno-assay (EIA) test kit (CHEKIT-
Toxotest, IDEXX Laboratories, Dr Bom-
meli AG, Switzerland) was used. The IFA
test slides contain the whole T. gondii
tachyzoites fixed in formalin, distributed
in 12 wells (Diagnostic & Technical Ser-
vices,Randburg,SouthAfrica).Onenega-
tive and 1 positive control were used on
each slide. The conjugate used was rabbit
anti-sheep immunoglobin G (IgG), with
affinity for purified antibody and fluo-
rescently labelled (Kirkegaard & Perry
Laboratories, Maryland, USA). Fluores-
cence at serum dilutions of 1:64 was con-
sideredpositive.Thiswasthetitreusedas
standard dilution for the IFA test by the
majority of similar studies11,15,18,22.
DatawereenteredintoMicrosoftExcel®
and then transferred to Epi-Info (Version
3.3.2., CDC Atlanta, 2005) for statistical
analysis.Quantitativedatawereanalysed
for significant correlations, with province
of origin, climate temperatures and man-
agement systems.
RESULTS
Sampling
A total of 600 samples was collected. Of
these, 278 originated from abattoirs and
322 were collected from rural farms.
Traceability: the origin of the sheep at
abattoirs and their destination after
slaughter, are shown in Table 1.
According to the Shoprite/Checkers
Supermarket Chain, mutton consump-
tion in various provinces of South Africa
washighestintheWesternCape(29.9%),
followedbyKwaZulu-Natal(24.1%),Gau-
teng (21.1 %) and Eastern Cape (12.6 %).
The lowest mutton consumption was
found in the Free State (6 %) (D Diemont,
Division Meat Markets, Shoprite/Check-
ers, pers. comm., 2006).
Analysis
The results of the serological tests are
summarised in Table 2.
Using the ELISA test, the seropreva-
lence shows some variation between
provinces, with a range of 2.7 % to 6.0 %.
The mean seroprevalence for all the
samples (n = 600) was 4.3 %.
Using the IFA test the seroprevalence
per province also varied, with a range of
2.7 % to 7.8 %. The mean seroprevalence
for South Africa, using the IFA test on the
sameserumsamples(n=600)was5.6%.
The agreement between the IFA test
andtheELISAtestwascalculatedas77%,
using the Kappa Test17.
The highest overall seroprevalence
among sheep tested was found in com-
mercial sheep (7.9 %, IFA), sampled at
abattoirs, while the lowest occurred in
sheep from rural farms (3.4 %, IFA). A
highly significant difference (P < 0.01)
between these 2 groups was found, with
an Odds Ratio of 0.4 (Table 3).
The seroprevalence of antibodies
Table 1: Origin of sheep and destination of meat.
Location of abattoir Origin of sheep Destination of mutton
Ladysmith (KZN) Ladysmith district (KZN)Ladysmith Butchery (KZN)
Cato Ridge (KZN)Summerville(EC)
Zastron (FS)
Durban Butchery (KZN)
Krugersdorp(G)Gauteng Central Meat Market, Krugersdorp (G)
Seemans, Randburg (G)
Broederstroom Butchery (G)
Bukeret (Pretoria) (G) Mpumalanga (MP)Johannesburg Butcheries (G)
Graaff-Reinet (EC) Graaff-Reinet (EC)Graaff-Reinet Butcheries (EC)
Port Elizabeth(EC) Grahamstown (EC)Port Elizabeth Butcheries (EC)
Steytlerville (EC)
East London (EC) Port Elizabeth (EC)East London Butcheries (EC)
Paarl (WC)Piketberg (WC)
Malmesbury (WC)
Moorreesburg (WC)
Cape Town Butcheries (WC)
Bethulie (FS) Colesberg (NC)
Bethulie (FS)
Bethulie Butchery (FS)
Durban Butcheries (KZN)
BrandfortBrandfort (FS)Brandfort Butchery (FS)
Table 2: Serological results from the ELISA test.
IFA ELISA
Province Prevalence per province in %Prevalence per province in %
KwaZulu-Natal
Eastern Cape
Western Cape
Gauteng
Free State
3.6
5.4
4.0
6.0
2.7
6.3
7.8
6.0
6.0
2.7
Table 3: Association between different farm types.
Type of sampleIFA ELISA
Pos*
Neg*
Pos*
Neg*
Abattoir samples
Rural samples
22
11
257
309
15 264
3137
Total33 566* 22 577*
Key:Pos = positive tests;Neg = negative tests, *Difference because 10 sera were insufficient volume for 2 tests
to be done.

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1180038-2809 Tydskr.S.Afr.vet.Ver. (2007) 78(3): 116–120
against T. gondii found in sheep sampled
in the 5 different provinces, with a differ-
ent minimum average and maximum
averagetemperature,isshowninTable4.
A significant correlation (P > 0.05) was
detected between the seroprevalence of
IgG in sheep and the minimum average
temperature (Table 5).
Sheep managed intensively had a
seroprevalence of 1.8 %, which was sig-
nificantly lower (P < 0.05) than the
seroprevalence in sheep under semi-
intensive management (5.3 %) (Table 6).
DISCUSSION
This study has shown the overall
seroprevalence of T. gondii in sheep in
South Africa to be 5.6 % (IFA test) and
4.3 % (ELISA). In neighboring countries,
such as Zimbabwe, an overall sero-
prevalence of 67.7 % was found in adult
sheep and goats7and in Botswana a
seroprevalence of 10 % was detected in
goats2. Compared with the data from
Zimbabwe, T. gondii seroprevalence in
South Africa is very low and closer to that
of Botswana, which, like South Africa, is
an arid country.
The consumption of mutton in South
Africa is highest in the Western Cape, fol-
lowed by KwaZulu-Natal and Gauteng
(D Diemont, Division Meat Markets,
Shoprite/Checkers, pers. comm., 2006).
Thehighconsumptionofmuttoninthese
2 provinces is possibly due to cultural dif-
ferencesinmeatconsumptionpatternsof
South African populations in different
provinces8.
The highest number of sheep in South
Africa is present in the Eastern Cape
(30.1 %), Northern Cape (25.3 %) and the
Free State (20.4 %)10. There is no agree-
ment between the consumption of mut-
tonperprovinceandthenumberofsheep
per province: the Western Cape with the
highest consumption of mutton has the
lowest number of sheep, while the East-
ern Cape which has the highest number
of sheep has a consumption of only
12.6 %. Considering this information, the
trace-back of sheep at the abattoirs can
be explained. KwaZulu-Natal receives
sheep for slaughtering from the Eastern
Cape and the Free State, which are the 2
provinces with the highest numbers of
sheep.
The study done on the seroprevalence
of T. gondii infection in sheep and goats in
Zimbabwe showed that sheep and goats
originating from commercial farms had
an 8 times lower seroprevalence (10 %)
compared with sheep and goats originat-
ing from rural areas (80 %)7. It was
expectedthatasimilarsituationwouldbe
seen in South Africa and therefore the
difference in seroprevalence between
rural and commercial farms was exam-
ined. As mentioned in the results, there
was a significantly higher seropreva-
lence in commercial then in rural farms
(P < 0.01). Only KwaZulu-Natal showed
a higher level in rural communities: 8.2 %
of the rural sheep population was sero-
positivecomparedwith4%ofsheepfrom
commercial farms. This province would
fit the picture given by the study done in
Zimbabwe by Hove et al.7,while the other
provinces show the opposite picture;
Eastern Cape (1.9 % rural and 11.5 %
urban),WesternCape(2%ruraland10%
urban) and Gauteng (3 % rural and 9.8 %
urban).
The different seroprevalences in the 5
provinces studied could be due to the
variations in temperature and humidity
in South Africa, ranging from a dry
climate in the northwest to a temperate
climateinthecentreandahumidtropical
climate along the southern and eastern
seaboard. The analysis of the minimum
averagedailytemperaturesinthe5study
areas revealed a significant correlation
between the seroprevalence of T. gondii
and this climatic factor (P < 0.05). The
Free State, with the lowest seropreva-
lence, has a minimum average daily tem-
peratureof8.6°C,whiletheEasternCape,
with the highest prevalence, has a mini-
mum average daily temperature of 13 °C.
Eastern Cape has the highest percentage
of infected sheep, followed by KwaZulu-
Natal, Western Cape and Gauteng. The
lowest prevalence of infected sheep was
found in the Free State. The coastal areas
of the Eastern and Western Cape and
KwaZulu-Natal have a mild and humid
climate, giving good conditions for
sporulation of T. gondii oocysts. This may
explain the lowest percentage (2.7 %) of
infected sheep found in the Free State,
which comprises mainly grassland with a
semi-aridclimate,withthelowminimum
average temperatures, likely to be unfa-
vourable for the sporulation of oocysts.
Previous epidemiological studies have
found infections in sheep to be more
prevalent in cool, moist areas than in hot,
dry areas13. Hove et al.7found similar
results in the study done in Zimbabwe: a
significantlyhigherseroprevalenceinthe
Mt Darwin and Bikita districts of Zimba-
bwe,whichreceiveahigherrainfall, com-
paredtothemorearidMudziandGwanda
districts.
Table 4: Seroprevalence of anti-Toxoplasma gondii antibodies in sheep sampled from
different climatic areas in South Africa.
Province Min average temperature
(°C)
Max average temperature
(°C)
% Infection
Gauteng
KwaZulu-Natal
Western Cape
Eastern Cape
Free State
10.4
14–17
8–14
14–17
8
24.3
25
23–25
20–23
20–23
6
6.3
6
7.75
2.7
Table 5: Analysis of minimum mean daily temperature.
Minimum mean daily
temperature (°C)
ELISA IFA
Pos*
Neg*
Pos*
Neg*
8–10
10–14
14–17
5 278
157
143
9 274
167
150
1012
127
Total 22 57833 567
Key: Pos = positive tests; Neg = negative tests.
Table 6: Comparison between different farm management systems.
Farm management
system
IFA ELISA
Pos*
Pos*
Neg*
Neg*
Extensive
Semi-intensive
10
23
5 273
305
268
29917
Total33 22 578567
Key:Pos = positive tests;Neg = negative tests, *Difference because 10 sera were insufficient volume for 2 tests
to be done.

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0038-2809 Jl S.Afr.vet.Ass. (2007) 78(3): 116–120119
Similar studies have also been done by
Van der Puije et al. who justified the
higher prevalence found in the wet
coastal savanna and the humid forest
zonesofGhana,asafactorresponsiblefor
the higher prevalence in these areas,
especially if compared with the drier
Guinea savanna of Ghana22. As variations
in humidity are also correlated to the
seroprevalence of T. gondii, the relatively
low rainfall in southern Africa might jus-
tify the much lower overall prevalence of
T. gondii in sheep in South Africa. South
Africa has an average annual rainfall of
464 mm, compared with a world average
of860mm19and,inaddition,SouthAfrica
isregularlyhitbydroughts,withthemost
recent one having occurred in 2004.
Another factor that increases the risk
of exposure of sheep to T. gondii is the
management system. Plant et al. sug-
gested that the prevalence of infection
was even more influenced by manage-
ment factors than by environmental fac-
tors14. In their study, a higher prevalence
was recorded in sheep kept under more
intensive systems of management and
they did not find a positive association
between the seroprevalence of T. gondii
in different geographical areas. Previous
epidemiological studies have found that
infections are more prevalent in sheep
kept under intensive or semi-intensive
systemsofmanagement15,23.VanderPuije
et al. associated the higher seropreva-
lence of T. gondii in sheep to the inten-
sive and semi-intensive farming system
in Ghana22. An association between
management and prevalence was also
observedinNorway16andintheUSA15.In
Tasmania, Munday concluded that the
seroprevalence of T. gondii was related to
the management system9. A similar trend
was found in the current study. The sero-
prevalence was high in the coastal areas
and in the urban areas (Gauteng) where
sheep-management practices were more
intensive compared with the Karoo area
and the Free State, which are character-
isedbytheirvast,extensivegrazingareas.
In a semi-intensive or intensive farming
system in South Africa, the sheep are
housed together entirely or partly during
the day. A possible explanation for the
higherprevalenceinthesesystems,could
be that domestic cats are more proba-
bly living near the food stores on such
farms,wheretheyareusedforcontrolling
rodents. For this reason sheep under
semi-intensive or intensive farming con-
ditions might be more exposed to Toxo-
plasma oocysts shed by cats. An experi-
mental study was done by Plant et al.
where an outbreak of ovine congenital
toxoplasmosis was simulated by feeding
sheepgraincontaminatedwithcatfaeces.
Their study confirmed that in an inten-
sive farming system, where cats are com-
monly kept on farms, feed could easily
be contaminated with oocysts and be
responsibleforarapidspreadofinfection
in a flock14.
CONCLUSIONS
The seroprevalence of T. gondii in sheep
in South Africa is lower than expected.
South Africans consume a relatively
large amount of mutton, especially mem-
bers of the Muslim community8. Informal
slaughtering is frequently practiced in
ruralareas.Itisestimatedthatabout30%
of sheep in South Africa are slaughtered
informally among the rural communities
mainlycomposedofsubsistenceorsmall-
scale farmers. In these communities,
many family members participate in the
slaughter process, the cleaning of the car-
cass or the preparation of the meat. Each
personinvolvedhasariskofbecomingin-
fected with T. gondii. In rural areas, the
lackofrunningwaterandthehabitofeat-
ing with the hands, further increases the
risk of becoming infected with T. gondii. It
isthusfortunatethat,althoughthatriskof
exposure to the parasite in mutton is
higher in the rural areas, the seropreva-
lence of toxoplasmosis was found to be
lower than in commercial sheep slaugh-
tered at abattoirs.
The consumption of undercooked
mutton and handling of raw meet during
the informal slaughter process is possibly
the main source of T. gondii infection for
humansinSouthAfrica.Thecontactwith
cats is a lower risk factor to South Afri-
cans, because the number of feral cats in
this country is relatively low. Informal
interviews with state veterinaries and
animal health technicians, as well as per-
sonal observations indicated that feral
catsarelesscommoninSouthAfricathan
inEurope.Catskeptaspetsmainlylivein
good hygienic conditions in urban areas
andarethereforenotconsideredasahigh
riskfactor.However,inordertoprovethis
statement it would be very interesting to
obtain more information on the sero-
prevalence of T. gondii in domestic and
feral cats and the role they play in the
epidemiology of toxoplasmosis in South
Africa.
ACKNOWLEDGEMENTS
Shoprite-Checkers Supermarket is ac-
knowledged with graditude for provid-
ing data on mutton consumption
patterns in South Africa. The University
ofPretoriaandtheNRFItaly-SouthAfrica
agreement are thanked for funding.
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