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Veterinary Parasitology: Regional Studies and Reports 22 (2020) 100456

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Veterinary Parasitology: Regional Studies and Reports


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Original Article

Seroepidemiology of Toxoplasma gondii in small ruminants in Northwest T


Ethiopia
Sisay Esubalewa, Zewdu Seyoum (Zed) Tarekegn Drb, , Wudu Temesgen Jemberu Drb,

Shimelis Dagnachew Nigatub, Mulugeta Kussab, Abrham Ayele Tsegayeb,


Girma Birhan Asteraye Drb, Basazinew Bogaleb, Mersha Chanie Kebede Profb
a
Estie District Livestock and Fishery Development Office, Amhara Regional state, Amhara, Ethiopia
b
The University of Gondar, College of Veterinary Medicine and Animal Sciences, Gondar, Ethiopia

ARTICLE INFO ABSTRACT

Keywords: This cross-sectional study with a cluster random sampling method was undertaken from November 2018 to May
Northwest Ethiopia 2019 to estimate the prevalence and assess the potential risk factors of T. gondii seropositivity, and to assess the
Risk factors association of the T. gondii seropositivity with reproductive losses in small ruminants in Northwest Ethiopia. A
Seroepidemiology total of 576 blood samples from 135 small ruminant flocks were collected and assayed for T. gondii IgG anti-
Small ruminants
bodies using the Toxo-latex slide agglutination test. A questionnaire survey was also conducted to gather in-
Toxoplasma gondii
formation on the potential risk factors of T. gondii seropositivity and on the status of reproductive losses in the
small ruminant flocks. The study demonstrated a high flock and animal level T. gondii seroprevalence of 96.3%
(95% CI: 91% - 98%) and 70.48% (95% CI: 68% - 79%), respectively. Mixed effect logistic regression analysis of
the potential risk factors showed that the odds of seropositive for T. gondii was significantly higher in sheep
(OR = 1.7, 95%CI: 1.19–2.46) than in goats, in adult (OR = 1.6, 95%, CI: 1.11–2.31) than in young, in the
presence of cats (OR = 2, 95%CI:1.32–3.04) than in the absence of cats, in the lack of knowledge on the role of
cats as a pathogen source than knowing it (OR = 1.82, 95% CI:1.21–2.77). The study also showed that the
likelihoods of experiencing the abortion, neonatal death and weak birth in the previous one year in T. gondii
seropositive flocks were 20.76 (95% CI: 2.2–195.1, p < 0.001), 8.90 (95% CI: 1.99–83.0, p = 0.021) and 9.33
(95% CI: 1.1–86.2, p = 0.019) times more than the seronegative flocks, respectively. In conclusion, this study
revealed high flock and animal level seroprevalence of T. gondii in the small ruminant population in northwest
Ethiopia, suggesting that lamb and goat might be a source of this pathogen for human infection if their infected
meat is consumed undercooked or uncooked. Besides, the observed association of T. gondii seropositivity with
reproductive losses may suggest the economic importance of the pathogen for the small ruminant producers.
Therefore, it warrants control attention to reduce its economic and public health burden in the study areas.
Further works on the economic impacts, bioassay, isolation, and genetic characterization of the pathogen are
suggested.

1. Introduction and 3) congenitally from infected mother to the fetus (Dubey, 2010).
Domestic cats and wild felids play a key role within the transmission
Toxoplasma gondii is an important food and waterborne obligate dynamics of the pathogen to humans and animals because they are the
intracellular protozoan parasite affecting animals and humans Dubey, sole definitive hosts that excrete environmentally resistant oocysts in
2009; Schlüter et al., 2014). Globally, it infects one-third of the human their faeces (Dubey, 2010). Infection in felines occurs mainly through
population and results in substantial health and economic concerns. the consumption of infected tissues from intermediate hosts (Dubey,
Food animals are sources of human infection (Dubey, 2010). Humans 2010; Robert-Gangneux and Dardé, 2012). The infection of cats and
can acquire the infection through 1) consumption of raw or under- other felids also occurs from the ingestion of sporulated oocysts.
cooked meat of food animals containing infective tissue cysts; 2) con- Toxoplasma gondii infection in the small ruminants may result in
sumption of contaminated food and water with environmental oocysts; congenital infections (related to embryonic death, fetal resorption/


Corresponding author.
E-mail address: Zewdu.seyoum@uog.edu.et (Z.S.Z. Tarekegn).

https://doi.org/10.1016/j.vprsr.2020.100456
Received 8 May 2020; Received in revised form 3 August 2020; Accepted 25 August 2020
Available online 29 August 2020
2405-9390/ © 2020 Elsevier B.V. All rights reserved.
S. Esubalew, et al. Veterinary Parasitology: Regional Studies and Reports 22 (2020) 100456

mummification, abortion, stillbirth or neonatal death) and reduced 2.3. Study design and sample size
flock milk production (Wang et al., 2011; Schlüter et al., 2014; Al-
Kappany et al., 2018); subsequently posing a possible challenge to the This cross-sectional study with a cluster random sampling was un-
small ruminant producers (Robert-Gangneux and Dardé, 2012). Meat dertaken from November 2018 to May 2019. The sample size was
from infected sheep and goats is a very important source of human calculated using a formula given by Dohoo et al. (2003). Expected
infection (Dubey, 2009) and thus pose a zoonotic risk because humans prevalence (Pexp) of 50%, desired absolute precision (d) of 5% and a
can acquire the pathogen from infected sheep and goats through raw or confidence level of 95% were considered for sample size calculation.
undercooked meat and milk consumption (Yang et al., 2012; Al- Therefore, 384 small ruminants were considered for sampling purposes.
Kappany et al., 2018). However, to account for the design effect associated with the clustering
Various studies have reported the seroprevalence of T. gondii in of study units within flocks and locations, the sample size was inflated
small ruminants across the world using different serological tests (Wang by 50% and that resulted in a total sample size of 576 small ruminants.
et al., 2011; Yang et al., 2012; Gebremedhin et al., 2013; Gazzonis
et al., 2015; Al-Kappany et al., 2018; Rasti et al., 2018; Sah et al., 2018; 2.4. Blood sample collection and serum separation
Bentum et al., 2019; Pereira et al., 2020). In Ethiopia, small ruminants
have been kept for income generation, sociocultural role, and animal Whole blood samples (about 3–5 ml) were collected aseptically
protein source, accounting for up to 35% of meat and 14% milk con- through jugular vein puncture using 10 ml plain vacutainer tubes. All
sumption in the country. Over 63 million heads of small ruminants are necessary information related to each animal: sex (female and male),
raised under diverse agro-ecological zones of Ethiopia (CSA, 2018); age (adult: > 1 year and young: ≤ 1 year), species (sheep and goat) and
however, geographically limited studies on T. gondii seropositivity have reproductive failure reports (abortion, stillbirth and fetal death) were
been done in the country (Negash et al., 2004; Teshale et al., 2007; properly labeled on blood collection tubes and the data recording sheet.
Gebremedhin et al., 2013; Zewdu et al., 2013; Tegegne et al., 2016; The blood samples were then allowed to clot in a slant position for a few
Tilahun et al., 2018) and particularly no seroprevalence study has been minutes and centrifuged at 4000 rpm for 5 min to separate the sera.
done in the northwest part of the country. The findings of these pre- Subsequently, sera were decanted into 1.5 ml Eppendorf tubes and kept
vious studies have shown that the seroprevalence of T. gondii antibodies at −20 °C until serological analysis for the presence of anti- T. gondii
in small ruminants ranges from 11.6% to 74.9% (Bekele and Kasali, antibodies.
1989; Teshale et al., 2007; Gebremedhin et al., 2013; Tegegne et al.,
2016). Within the country, the causes of most reproduction losses 2.5. Questionnaire survey
(abortion, stillbirth and neonatal deaths) within the flocks of small
ruminants are not well documented and also the association with the A pretested semi-structured questionnaire survey was conducted
seroprevalence of T. gondii has not been well noted (Teshale et al., during blood sample collection by interviewing owners or attendants to
2007; Gebretensay et al., 2019). Data on the seroprevalence of T. gondii assess the potential risk factors for T. gondii infection in sheep and goat
in small ruminants would be caring for planning and implementing population. The hypothesized potential risk factors for T. gondii such as
precautionary measures for public health and economic impacts. having knowledge on the role of a cat as a source of a pathogen (yes/
Therefore, the objectives of our study were: 1) to estimate the ser- no), altitude (highland: ≥ 2300, midland: 1500–2300 and low-
oprevalence and the possible risk factors of Toxoplasma gondii infection land: ≤ 1500 m above sea level (m.a.s.l)), flock size (≤ 10, 11–20
in small ruminants in Northwest Ethiopia and 2) to assess the re- and > 20), presence of house as well as feral cats in or around the
lationship of seropositivity for T. gondii with reproductive losses in the household (yes/no), presence of rodents and wild feline in the house-
small ruminants. hold (yes/no), cat-feed sources (raw animal product, cooked animal
product, household leftover or hunting), dead animal disposal method
2. Materials and methods (buried, feeding for cat and dog or throw away in the field), and animal
feed contamination by cat faces (yes/no) were assessed. Also, previous
2.1. Study areas experiences of owners/attendants about the occurrence of reproductive
losses in breeding animals at flock or a household level were inter-
The study was conducted in Estie and Gondar- Zuria districts, viewed. Thus, reproductive failures such as a history of abortion (yes/
Amhara regional state, northwest Ethiopia. Estie district is situated at no), neonatal death (yes/no) and weak birth (yes/no) over the previous
11°39′59.99” N latitude and 38°09′60.00″ E longitude with an altitude one year were recorded.
ranging from 1500 to 3420 m above sea level. The district annual
temperature and rainfall range from 8.3 °C - 25 °C and 1307-1500 mm, 2.6. Serological analysis
respectively. According to Estie district Animal Resource and Health
Care Office (EDARHCO, 2017); its livestock population comprises about Toxoplasma gondii antibodies were assayed in the collected serum
176,737 cattle, 86,487 sheep, 66,696 goats, and 39,938 equines. samples using the Toxo-latex slide agglutination test (SPINREACT, S.A/
Gondar-Zuria district: is also located at 12° 40′ 0″ N latitude and 37° 20′ S.A.U, GIRONA, SPAIN) following the previous reports (Ibrahim et al.,
0″ E longitude with an altitude ranges from 1966 to 2133 m above sea 2014; Tegegne et al., 2016) and manufacturer's recommendations.
level. The district average minimum and maximum annual temperature Agglutinates were detected using the naked eye and stereomicroscope.
and rainfall range from 24 °C–33 °C and 950 - 1035 mm, respectively. The presence of agglutination was considered as positive at a titer of
According to the Gondar-Zuria District Agricultural office (2015) ≥1:2 and indicates an antibody concentration equal to or greater than
GZDAO, 2015, the livestock population in the district includes 212,164 4 IU/ml. The herd also considered when at least one animal was found
cattle, 75,324 sheep, 97,640 goats, 28,345 equines, and 173,391 do- positive. The laboratory procedures were performed at the University of
mestic chickens. Gondar, College of Veterinary Medicine and Animal Sciences, Veter-
inary Parasitology Laboratory.
2.2. Study animals
2.7. Data management and analysis
The study animals were indigenous sheep and goats kept under
extensive management in the mixed crop-livestock production system The data generated was stored in the Microsoft Excel spreadsheet
of the area. Animals, which six and above months of age were included (2010) and analyzed using STATA Version14 software for windows.
in the sampling process. The data were summarized using descriptive statistics. Seroprevalence

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Table 1
Univariable and multivariable mixed-effect logistic regression analysis of potential risk factors for Toxoplasma gondii.
Variables Category No. of No. of Prevalence% Univariable Multivariable
examined positive (95%CI)
COR (95% CI) P-value AOR (95%CI) P-value

Species Goat 281 182 65 (0.59–0 0.70) 1.0


Sheep 295 224 76 (0.71–0.80) 1.72(1.19–2.47) 0.003 1.90(1.28–2.82) 0.001
Sex Male 131 89 68 (0.59–0.75) 1.0
Female 445 317 71 (0.67–0 0.75) 1.16(0.77–1.78) 0.467
Age Young 209 134 64 (0.57–0 0.70) 1.0
Adult 367 272 74 (0 0.69–0.78) 1.6(1.11–2.31) 0.011 1.76(1.20–2.58) 0.004
Altitude Low land 80 53 66 (0.55–0.75) 1.0
Mid land 354 250 71 (0.66–0.75) 1.2(0.7–2.0) 0.442
High land 142 103 73.5 (0.65–0.79) 1.3(0.7–2.3) 0.326
Dead animal disposal Buried 40 11 28 (0.15–0.43) 1.0
Feeding for cat 435 316 73 (0.68–0.77) 7(3.3–14.4) < 0.001
Throw away 49 39 80(0.65–0.89) 10(3.8–27.4) < 0.001
Cat feed source Cooked animal 45 10 22.2 (0.12–0.37) 1.0
product
Hunting 188 139 73.9 (0.67–0.79) 9.92(4.58–21.55) < 0.001
Household left over 101 81 80.1 (0.71–0.87) 14.17(6.02–33.38) < 0.001
Raw animal product 123 107 86.9 (0.79–0.92) 23.4(9.73–56.29) < 0.001
Knowledge on the cat as a pathogen Yes 398 266 67 (0.62–0.71) 1.0
sources No 178 140 77 (0.72–0.84) 1.82(1.21–2.77) 0.004 1.89(1.22–2.92) 0.004
Flock size ≤ 10 239 166 69(0.63–0.75) 1.0
11–20 195 139 71(0.65–0.77) 1.09(0.72–1.67) 0.679
> 20 142 101 71(0.63–0.78) 1.08(0.68–1.79) 0.731
Cat-feed contamination No 92 62 67 (0.57–0.76) 1.0
Yes 364 274 75 (0.71–0.79) 1.47(0.91–2.42) 0.125
Feral cat presence No 226 159 70 (0.64–0.76) 1.0
Yes 350 247 71 (0.66–0.75) 1.01(0.70–1.46) 0.955
Cat presence No 120 70 58 (0 0.49–0.67) 1.0
Yes 456 336 74 (0.69–0.78%) 2(1.32–3.04) 0.001 1.70(1.09–2.64) 0.018
Wild feline presence No 162 182 65 (0.56–0.71) 1.0
Yes 414 224 76 (0.68–0.77) 1.50(1.02–2.22) 0.038

COR = crude odds ratio, AOR = adjusted odds ratio.

of T. gondii infection was calculated by dividing the total number of 3. Results


seropositive animals to the total number of examined animals.
Similarly, flock level seroprevalence was calculated as the number of 3.1. Questionnaire survey on potential risk factors for Toxoplasma infection
flocks with at least one positive animal divided by the total number of
flocks tested. Mixed effect logistic regression analysis was used to A total of 135 small ruminant owners/attendants participated in the
identify potential risk factors associated with Toxoplasma seropositivity. questionnaire survey aimed at collecting data about potential risk fac-
First, a univariable logistic regression analysis with the flock as a tors for toxoplasmosis. Out of 135 respondents, 87.75% did not know
random effect was done was made and potential risk factors (ex- concerning the role of a cat as a pathogen source. All of them practiced
planatory variables) with p-values ≤0.25 were screened for the mul- an extensive management system. Among the respondents, 84.4% had a
tivariable mixed-effect logistic regression. Before running the multi- cat in their homes. The most frequently mentioned feed sources for
variable mixed-effect logistic model, the explanatory variables were domestic cat was hunting (34%) followed by household leftover (32%),
checked for multicollinearity using the variance inflation factor (VIF), raw animal product (26%) and cooked animal product (8%).
and a variance inflation factor value of greater than 10 was considered Respondents also stated that wild felines (67%) and feral cats (86%)
the cut-off point for the collinearity diagnostics (Johnston et al., 2018). present in the area and around their home. Of the respondents, 54% of
The associations were considered statistically significant when them stated that the time of abortion for sheep and goats was mostly in
P < 0.05 at 95% confidence level. Odds ratios (OR) at a 95% con- the early gestation period while 19% of them said in mid-gestation and
fidence interval (CI) were used to express the strength of the risk of the 27% in the last gestation. In the study areas, farmers disposed of dead
diseases associated with the tested factors. Association of reproductive animals in different ways, such as burying (8%), feeding for cat and dog
losses (abortion, neonatal death, and weak birth) with seropositivity for (31%), and throw away in the environment (61%).
T. gondii at flock level was analyzed similarly using mixed-effect logistic
regression considering reproductive flosses as outcome variables and 3.2. Seroprevalence and risk factor analysis
seropositivity as the explanatory variable.
3.2.1. Flock and animal level seroprevalence
In the current study, a total of 576 small ruminants' sera from 135
2.8. Ethical consideration flocks were assayed by Toxo-latex slide agglutination test. The overall
IgG seropositivity for T. gondii was found 96.29% (95% CI: 91% - 98%)
Ethical approval for the study protocol was obtained from the and 70.48% (95% CI: 68% - 79%) at flock and animal level, respec-
Institutional Review Board of the University of Gondar (reference letter tively. Higher animal level seroprevalence was recorded in Estie 74%
No: O/V/P/RCS/05/1237/2018; On May 16, 2018). Samples and other (95% CI: 68% - 78%) than in Gondar- Zuria district 67% (95%CI: 61% -
available data were taken from owners after informed consent ex- 72%). However, the difference was not statistically significant
plaining the purpose, benefit, and possible risks of the study. (p > 0.05). Seroprevalence of T. gondii in young sheep (70%; 95%CI:
61% - 77.6%) was significantly (p < 0.05) lower than in adult sheep
(80%; 95%CI: 73% - 86%). Similarly, it was significantly (p = 0.020)

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lower in young goats (54%; 95% CI: 43% - 65%) than in adult goats Africa (Fereig et al., 2016; Bentum et al., 2019), from Asia (Wang et al.,
(69%; 95%CI: 62% - 75%). 2011; Rasti et al., 2018; Bachan et al., 2018; Sah et al., 2018;
Pagmadulam et al., 2020) and Europe (Cenci-Goga et al., 2013; García-
3.2.2. Analysis of risk factors Bocanegra et al., 2013; Lopes et al., 2013). We hypothesized that many
From the total of 12 potential risk factors considered in the uni- factors attributed to this variation among reports such as diagnostic
variable logistic regression analysis, species, age, the presence of cats tests used and their cut-off values, geographical and climate variations,
and wild felines, cat feeding sources, dead animal disposal methods and hygienic status difference, presence and relative density of the cat po-
knowledge on the role of a cat as pathogen source showed association pulation, access of contaminated feed and water to the study animals,
with of T. gondii with p < 0.25 (Table 2) and qualified for the risk sample size and management system.
factor analysis using the multivariable mixed-effect logistic recession Species of small ruminants have shown a significant effect on the
analysis. seropositivity for T. gondii. Sheep had higher seropositivity for anti- T.
Among those potential risk factors screed for multivariate logistic gondii antibodies (76%) than in goats (67%). Published reports gen-
regression analysis cat feed sources, animal feed contamination by cat erally show that the prevalence in sheep is higher than in goats (García-
faces, and dead animal disposal methods were removed from the model Bocanegra et al., 2013; Lopes et al., 2013; Fereig et al., 2016; Rasti
because of multi-collinearity with cat's presence. In the multivariable et al., 2018). This conforms to the previous reports in Ethiopia (Negash
analysis, age, species, the presence of a cat, and knowledge on the role et al., 2004; Gebremedhin et al., 2013, 2014; Gebremedhin and Gizaw,
of the cat as a pathogen source found to have a statistically significant 2014; Tegegne et al., 2016; Tilahun et al., 2018) and across the globe
effect on the seropositivity for T. gondii in the small ruminant popula- (Tzanidakis et al., 2012; Gazzonis et al., 2015; Bentum et al., 2019;
tion (p < 0.05). The risk of acquiring T. gondii infection was higher in Tagwireyi et al., 2019; Pagmadulam et al., 2020). This might be as-
adult than young (OR = 1.76), in sheep than goat (OR = 1.90), in the cribed to the differences in feeding behavior because sheep are more
presence of cat than the absence of cat (OR = 1.70), in lack of likely to acquire sporulated oocysts from the pasture during grazing
knowledge on the role of the cat as a pathogen source than knowl- close to the soil than goats which have a preference for browsing. On
edgeable (OR = 1.89) (Table 1). the other hand, authors from elsewhere in the world had documented a
higher prevalence in goats than in sheep (Abu-Dalbouh et al., 2012; Al-
3.3. Association of Toxoplasma gondii seropositivity with reproductive Kappany et al., 2018; Tonouhewa et al., 2019; Pereira et al., 2020).
losses According to these authors, this might be associated with herding
practices and the behavior of caprine since they are accustomed to
Reproduction losses (abortion, neonatal death, and weak birth) higher activity and movement that increases the probability of contact
identified in this study were significantly associated with seropositivity with contaminated sources, although these require further investiga-
for T. gondii (P < 0.05). The likelihoods of experiencing the abortion, tion.
neonatal death, and weak birth in the previous one-year in the ser- In the current survey, age has also shown a significant association
opositive flocks were 20.76, 8.9, and 9.33 times more than seronegative with anti-Toxoplasma gondii antibodies seropositivity. The adult animals
flocks, respectively (Table 2). were 1.6 times more prone to seropositivity for anti- T. gondii antibodies
than young animals. Similar results were also confirmed by
Gebremedhin et al. (2013a), Zewdu et al. (2013), Gebremedhin et al.
4. Discussion
(2014), Gazzonis et al. (2015), Tegegne et al. (2016), Sah et al. (2018)
and Pereira et al. (2020). This variation might be attributed to the
Small ruminants (sheep and goat) are important animal protein
cumulative effect of age as compared with younger animals. Older
sources (meat and milk) and play a crucial role in the food and nutrition
animals are more likely to acquire repeatedly the sporulated oocysts
security in Ethiopia. However, products derived from these animals
from the environment as they lived longer. Other previous reports have
could be important sources of zoonotic disease pathogens. One of such
also shown a higher exposure risk associated with increasing age
zoonotic disease pathogens is Toxoplasma gondii. As intermediate hosts,
(Teshale et al., 2007; Bachan et al., 2018; Sah et al., 2018; Tilahun
small ruminants are important sources of T. gondii for human infection.
et al., 2018).
This study has indicated the widespread occurrence of T. gondii infec-
The risk factor analysis further showed a significant effect of having
tion in the small ruminant population in northwest Ethiopia with a high
a cat in the household on the seropositivity for T. gondii in the study
flock and animal level seroprevalence of 96.29% and 70.48%, respec-
animals (p < 0.05). This suggests that cats could be important sources
tively. This coincides with the previous studies in Ethiopia, which si-
of T. gondii for hosts such as grazing animals through infectious oocysts
milarly reported high seroprevalence of T. gondii in small ruminants
contamination of the environment. This finding is consistent with
(Negash et al., 2004; Teshale et al., 2007; Tegegne et al., 2016). Simi-
previous studies (Abu-dalbouh et al., 2012; Deng et al., 2016; Al
larly, the present findings are compatible with the reports of Hove et al.
Hamada et al., 2019). The presence of cats is imperative in the life cycle
(2005) from Zimbabwe, Al-Kappany et al. (2018) from Egypt, Pereira
of T. gondii and results in increasing seroprevalence among inter-
et al. (2020) from Sao-Tome and Principe, and Gazzonis et al. (2015)
mediate hosts in various studies (Dubey, 2010).
from Italy. But, the present finding is higher than some other previous
Although feral cats are important in the epidemiology of Toxoplasma
reports from Ethiopia (Gebremedhin et al., 2013, Gebremedhin et al.,
gondii, it is astonishing that the seropositivity in small ruminants was
2013a, 2014; Zewdu et al., 2013; Gebremedhin and Gizaw, 2014), from

Table 2
Reproductive lose status of flocks and the association between reproductive loses and Toxoplasma seropositivity.
Reproductive loss. No. of flocks Toxoplasma seropositivity % (95% CI) OR (95%CI) P-value

Abortion Yes 110 99 (93.7–99.9) 20.76 (2.2–195.1) 0.0003

No 25 84 (63.6–94.0)
Neonatal death Yes 91 98.9 (92.0–99.8) 8.90 (1.99–83.0) 0.021
No 44 90.9 (77.8–96.6)
Weak birth Yes 92 98.9 (92.5–99.8) 9.33 (1.1–86.2) 0.019
No 43 90.6 (77.3–96.5)

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not significantly associated with the presence of feral cats. This might toxoplasmosis (Toxoplasma gondii) in aborted animals in Jordanian goat and sheep
be because in flocks where feral cats absent in the surrounding, flocks. Trop. Anim. Health Prod. 44 (1), 49–54. https://doi.org/10.1007/s11250-
011-9885-2.
household cats and wild felids would access and contaminate the feed Ahmed, Y.F., Sokkar, S.M., Desouky, H.M., Soror, A.H., 2008. Abortion due to tox-
and water sources of animals. Moreover, according to Tzanidakis et al. oplasmosis in small ruminants. Glob. Vet. 2 (6), 337–342.
(2012), farmers might not notice feral cats around their house or on the Al Hamada, A., Habib, I., Barnes, A., Robertson, I., 2019. Risk factors associated with
seropositivity to Toxoplasma among sheep and goats in northern Iraq. Vet. Parasitol.
grazing areas, which can be responsible for the contamination of pas- Reg. Stud. Rep. 15, 100264. https://doi.org/10.1016/j.vprsr.2019.100264.
tures or feed and water sources. Al-Kappany, Y.M., Abbas, I.E., Devleesschauwer, B., Dorny, P., Jennes, M., Cox, E., 2018.
Toxoplasma gondii infection in sheep and goats can cause embryo/ Seroprevalence of anti-Toxoplasma gondii antibodies in Egyptian sheep and goats.
BMC Vet. Res. 14 (1), 120. https://doi.org/10.1186/s12917-018-1440-1.
fetal resorption or mummification, abortion, stillbirth, fetal death, the Bachan, M., Deb, A.R., Maharana, B.R., Sudhakar, N.R., Sudan, V., Saravanan, B.C.,
birth of a weak lamb or kid (Pavlović and Ivanović, 2005; Givens and Tewari, A.K., 2018. High seroprevalence of Toxoplasma gondii in goats in Jharkhand
Marley, 2008; Abu-Dalbouh et al., 2010). This study demonstrated a state of India. Vet. Parasitol. Reg. Stud. Rep. 12, 61–68. https://doi.org/10.1016/j.
vprsr.2018.02.004.
significant association between flocks having a history of reproductive
Bekele, T., Kasali, O.B., 1989. Toxoplasmosis in sheep, goats and cattle in Central
losses (abortion, neonatal death, and weak birth) and flock level ser- Ethiopia. Vet. Res. Commun. 13 (5), 371–375. https://doi.org/10.1007/bf00346069.
opositivity for T. gondii (P < 0.05). Similar findings were reported by Bentum, K.E., Folitse, R.D., Amemor, E., Burimuah, V., Opoku-Agyemang, T., Emikpe,
Gebremedhin et al. (2013) and Heidari et al. (2013). In our study, B.O., 2019. Seroprevalence of Toxoplasma Gondii antibodies in sheep and goats
slaughtered at the Kumasi abattoir, Ghana. J. Immunoass. Immunochem. 40 (5),
99.9% of flocks having a history of abortion resulted in T. gondii posi- 495–501. https://doi.org/10.1080/15321819.2019.1642916.
tive reaction. This finding is supported by Ahmed et al. (2008) who Borde, G., Lowhar, G., Adesiyun, A.A., 2006. Toxoplasma gondii and Chlamydophila abortus
reported as all aborted ewes and does reveal a positive reaction for T. in caprine abortions in Tobago: a sero-epidemiological study. J. Vet. Med. B Infect.
Dis Vet. Public Health 53 (4), 188–193. https://doi.org/10.1111/j.1439-0450.2006.
gondii infection. Moreover, Abu-Dalbouh et al. (2012) also revealed that 00931.x.
from 93 flocks that had cases of abortion, 40 flocks (43%) had at least Caldeira, F.H.B., Ubiali, D.G., Godoy, I.D., Dutra, V., Aguiar, D.M.D., Melo, A.L.T., Riet-
one T. gondii PCR-positive animal. On the other hand, in Ethiopia, Correa, F., Colodel, E.M., Pescador, C.A., 2011. Outbreak of caprine abortion by
Toxoplasma gondii in Midwest Brazil. Pesqui. Vet. Bras. 31 (11), 933–937.
neonatal losses have been reported to be higher from T. gondii infection Cenci-Goga, B.T., Ciampelli, A., Sechi, P., Veronesi, F., Moretta, I., Cambiotti, V.,
in sheep (Gebremedhin et al., 2013; Gebretensay et al., 2019); thus the Thompson, P.N., 2013. Seroprevalence and risk factors for Toxoplasma gondii in sheep
findings are supported by our report. This is strengthened in the as- in Grosseto district, Tuscany, Italy. BMC Vet. Res. 9, 25. https://doi.org/10.1186/
1746-6148-9-25.
sertion that parasite is one of the main causes of abortion, neonatal CSA (Central Statistical Authority), 2018. Agricultural Sample Survey, Statistical Bulletin,
losses, and weak birth in sheep and goat population (Dubey, 2009; and Addis Ababa, Ethiopia.
Caldeira et al., 2011). Borde et al. (2006) also observed T. gondii de- Deng, H., Dam-Deisz, C., Luttikholt, S., Maas, M., Nielen, M., Swart, A., Vellema, P., van
der Giessen, J., Opsteegh, M., 2016. Risk factors related to Toxoplasma gondii ser-
creases the fertility rate of goats and increase mortality and abortion
oprevalence in indoor-housed Dutch dairy goats. Prevent. Vet. Med. 124, 45–51.
rate. https://doi.org/10.1016/j.prevetmed.2015.12.014.
In conclusion, the current study revealed high seroprevalence of T. Dohoo, I., Martin, W., Stryhn, H., 2003. Veterinary Epidemiologic Research, 2nd ed. AVC
gondii in the small ruminant population in northwest Ethiopia, sug- Inc, Charlottetown, Prince Edward Island, Canada.
Dubey, J.P., 2009. Toxoplasmosis in sheep–the last 20 years. Vet. Parasitol. 163 (1–2),
gesting that lamb and goat might be a source of this pathogen for 1–14. https://doi.org/10.1016/j.vetpar.2009.02.026.
human infection if their infected meat is consumed undercooked or Dubey, J.P., 2010. Toxoplasmosis of Animals and Humans. CRC Press, Boca Raton.
uncooked. Species, age, cat's presence around the farm, and knowledge https://doi.org/10.1201/9781420092370.
EDARHCO, 2017. Estie District Animal Resource and Health Care Office (2017): Annual
on the role of the cats as pathogen sources were identified as risk factors Report of 2017.
for T. gondii seropositivity. The study also demonstrated seropositivity Fereig, R.M., Mahmoud, H., Mohamed, S., AbouLaila, M.R., Abdel-Wahab, A., Osman,
for T. gondii was associated with reproductive losses with an important S.A., Zidan, S.A., El-Khodary, S.A., Mohamed, A., Nishikawa, Y., 2016.
Seroprevalence and epidemiology of Toxoplasma gondii in farm animals in different
economic consequence for flock owners. Therefore, it warrants control regions of Egypt. Vet. Parasitol. Reg. Stud. Rep. 3-4, 1–6. https://doi.org/10.1016/j.
attention to reduce its economic and public health concerns. Further vprsr.2016.05.002.
works on the economic impacts, bioassay, isolation, and genetic char- García-Bocanegra, I., Cabezón, O., Hernández, E., Martínez-Cruz, M.S., Martínez-Moreno,
Á., Martínez-Moreno, J., 2013. Toxoplasma gondii in ruminant species (cattle, sheep,
acterization of the pathogen are suggested.
and goats) from southern Spain. J. Parasitol. 99 (3), 438–440. https://doi.org/10.
1645/12-27.1.
Ethical statement Gazzonis, A.L., Veronesi, F., Di Cerbo, A.R., Zanzani, S.A., Molineri, G., Moretta, I.,
Moretti, A., Piergili Fioretti, D., Invernizzi, A., Manfredi, M.T., 2015. Toxoplasma
gondii in small ruminants in northern Italy - prevalence and risk factors. Annal.
Ethical approval for the study protocol was obtained from the Agricult. Environ. Med. AAEM 22 (1), 62–68. https://doi.org/10.5604/12321966.
Institutional Review Board of the University of Gondar (reference letter 1141370.
No: O/V/P/RCS/05/1237/2018; On May 16, 2018). Samples and other Gebremedhin, E.Z., Gizaw, D., 2014. Seroprevalence of Toxoplasma gondii infection in
sheep and goats in three districts of southern nations, nationalities and peoples’ re-
available data were taken from owners after informed consent ex- gion of Ethiopia. World Appl. Sci. J. 31 (11), 1891–1896. https://doi.org/10.5829/
plaining the purpose, benefit and possible risks of the study. idosi.wasj.2014.31.11.83312.
Gebremedhin, E.Z., Agonafir, A., Tessema, T.S., Tilahun, G., Medhin, G., Vitale, M., Di
Marco, V., 2013. Some risk factors for reproductive failures and contribution of
Declaration of Competing Interest Toxoplasma gondii infection in sheep and goats of Central Ethiopia: a cross-sectional
study. Res. Vet. Sci. 95 (3), 894–900. https://doi.org/10.1016/j.rvsc.2013.08.007.
Gebremedhin, E.Z., Agonafir, A., Tessema, T.S., Tilahun, G., Medhin, G., Vitale, M., Di
We have no conflict of interest with this manuscript or report. Marco, V., Cox, E., Vercruysse, J., Dorny, P., 2013a. Seroepidemiological study of
ovine toxoplasmosis in east and west Shewa zones of Oromia regional state, Central
Acknowledgements Ethiopia. BMC Vet. Res. 9, 117. https://doi.org/10.1186/1746-6148-9-117.
Gebremedhin, E.Z., Abdurahaman, M., Hadush, T., Tessema, T.S., 2014. Seroprevalence
and risk factors of Toxoplasma gondii infection in sheep and goats slaughtered for
We would like to thank the owners of sheep and goats who allowed human consumption in Central Ethiopia. BMC Res. Note 7, 696. https://doi.org/10.
collecting blood samples from their animals. We would also like to 1186/1756-0500-7-696.
Gebretensay, A., Alemayehu, G., Rekik, M., Alemu, B., Haile, A., Rischkowsky, B., Aklilu,
acknowledge the Office of Vice President for Research and Community
F., Wieland, B., 2019. Risk factors for reproductive disorders and major infectious
Service, the University of Gondar for its financial support. causes of abortion in sheep in the highlands of Ethiopia. Small Rumin. Res. 177, 1–9.
https://doi.org/10.1016/j.smallrumres.2019.05.019.
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