Veterinary Parasitology: Regional Studies and Reports 22 (2020) 100475

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Veterinary Parasitology: Regional Studies and Reports

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Original Article

First report of Toxoplasma gondii infection and associated risk factors in the T
dromedary camel (Camelus dromedarius) population in south East Algeria
Mohamed-Cherif Abdallaha, Miroud Kamelb, Benfodil Karimaa, Ansel Samira,
Benaissa Mohammed Hocinec, Khelef Djamela, Kaidi Rachidd, Ait-Oudhia Khatimaa,d,
⁎

a
Ecole Nationale Supérieure Vétérinaire d'Alger. BP 161. Issad Abbes, Oued Smar, Alger, Algeria
b
Laboratoire « Epidémio-surveillance, santé, productions et reproduction, expérimentation et thérapie cellulaire des animaux domestiques et sauvages (ESSPRETCADS) »,
Institut des Sciences Vétérinaires, Université Chadli Bendjedid El-Tarf, Algeria
c
Centre de Recherche Scientifique et Technique sur les Régions Arides (CRSTRA), Touggourt, Algeria
d
Laboratoire des Biotechnologie et Reproduction Animale (LBRA), Institut des Sciences Vétérinaires Blida, Algeria

ARTICLE INFO ABSTRACT

Keywords: The study aimed at assessing the prevalence of toxoplasmosis due to T. gondii in dromedaries by the ELISA test
Toxoplasma gondii and to identify associated risk factors. A cross-sectional study was performed on 320 dromedaries (Camelus
Camelus dromedarius dromedaries) from January to March 2018 in four provinces of southeastern Algeria (Biskra, El- Oued, Ouargla,
Prevalence and Ghardaia). A structured questionnaire was used to collect data on individual characteristics, husbandry
ELISA
management and health conditions. The ELISA test revealed an overall seroprevalence of 15% (CI95%:
Risk factors
11.5–19.33). Possible factors associated with T. gondii infection were analyzed by univariate analysis and
Algeria
multivariate logistic regression. Age, husbandry system, and study area were identified as risk factors for T.
gondii infection. Increased seropositivity was observed in old animals older than 10 years (OR = 2.81; CI:
1.51–3.87; p = 0.003), two times higher in animals living in the intensive husbandry system (OR = 2.42; CI:
1.3–3.07; p = 0.003), and four times higher in animals living in Biskra (OR = 4.2; CI: 1.21–9.85; p = 0.0001)
than other provinces. The identification of the risk factors determines the type of measures and strategies to be
applied to reduce, control and prevent T. gondii infection in dromedaries and thereby reducing human infection
risks.

1. Introduction contract T. gondii infection by ingestion or inhalation of sporulated

Camelidae are an important animal production resource in many
areas of the world. The reproductive efficiency of camelids is generally
considered low (Kaufmann, 2005; Tibary and Anouassi, 1997). In
dromedaries (Camelus dromedarius), birth rates rarely exceed 40% in
nomadic herds and 70% in more intensive herds (Tibary et al., 2005;
Tibary and Anouassi, 1997). Camels suffer from various abortion-
causing diseases, including brucellosis (Wernery, 1991; Zowghi and
Ebadi, 1988), placentitis or uterine infections (Enany et al., 1990;
Wernery, 1991; Wernery et al., 1992; Yadm and Ragab, 1994), tox­
oplasmosis (Hagemoser et al., 1990), trypanosomosis (Karimi and
Kimenye, 1990; Egbe-Nwiyi and Chaudhry, 1994; Tibary and Anouassi,
1997) and camel pox (Abdi-Arush, 1982).
Toxoplamosis is caused by an intracellular protozoan of
Apicomplexa, T. gondii, which is present worldwide and in a very wide
range of hosts (Boothroyd and Grigg, 2002; Dubey, 2010). Camels
oocysts that infected wild cats or felids release into the environment
(Elamin et al., 1992). People, especially those leaving in transhumant
and pastoral communities, become infected by ingesting raw and un­
dercooked meat of infected animals (Dubey, 2010) and by ingesting
raw milk contaminated with oocysts (Saad et al., 2018). Controlling
toxoplasmosis is vital for it can seriously decrease the quality of life and
even lead to death in humans as well as in animals. It also impacts the
wildlife and the ecosystem health (Aguirre et al., 2019).
In southern Algeria, dromedary camels play an important role in the
agricultural economy. Most of them are reared according to traditional
farming practices that are characterized by very poor hygiene condi­
tions and a close contact with many different species of animals, in­
cluding wild, and domestic felines. Recent health studies in Algeria
report a high seroprevalence (50 to 55%) of toxoplasma serology in
women of childbearing age (Berredjem et al., 2017; Messerer et al.,
2014).

⁎
Corresponding author at: Ecole Nationale Supérieure Vétérinaire d'Alger, BP 161. Issad Abbes, Oued Smar, Alger, Algeria.
E-mail addresses: khatima.aitoudhia@gmail.com, k.aitoudhia@ensv.dz (A.-O. Khatima).

https://doi.org/10.1016/j.vprsr.2020.100475
Received 9 March 2020; Received in revised form 21 August 2020; Accepted 22 September 2020
Available online 24 September 2020
2405-9390/ © 2020 Elsevier B.V. All rights reserved.
M.-C. Abdallah, et al.
Fig. 1. Distribution of seroprevalence of Toxoplasma gondii infection in southeastern Algeria.
Cases of T. gondii infection have been reported in Camelus drome­
darius in several countries (Dubey and Beattie, 1988; Dubey, 2010). The
prevalence of T. gondii infection in camels varies considerably from one
area to another of the world (Shaapan and Khalil, 2008), ranging from
3.12% in Iran (Dehkordi et al., 2013) to 90.90% in Turkey (Utuk et al.,
2012). This study was carried out to determine the prevalence of tox­
oplasma antibodies among dromedaries and assess the risk factors that
are associated with this infection in dromedaries' herds in southeast
Algeria.
2. Materials and methods
2.1. Study area
This study took place in four provinces (Biskra, El- Oued, Ouargla,
and Ghardaia) in southeastern Algeria. The wilayates of the study were
chosen because of their high concentration in dromedaries farming and
the significant development in the consumption of camel meat and milk
by the local population (Fig. 1).
- In Ghardaia, the average high-temperature is 41.7 °C (107.1 °F) and
the average low-temperature, is 25.5 °C (77.9 °F). The average re­
lative humidity is 25.9% and during the entire year, the rain falls for
24 days and up to 61.4 mm (2.4″) of precipitation.
- In Biskra, the average high-temperature is 39.6 °C (103.3 °F) and the
average low-temperature, is 27.3 °C (81.1 °F). The average relative
humidity is 30.1% and during the entire year, the rain falls for
35.5 days and up to 128.8 mm (5.1″) of precipitation.
2
Veterinary Parasitology: Regional Studies and Reports 22 (2020) 100475
- In El-Oued, the average high-temperature is 39 °C (104 °F) and the
average low-temperature, is 21.8 °C (74.2 °F). The average relative
humidity is 24.3% and during the entire year, the rain falls for
24 days and up to 74 mm (2.9″) of precipitation.
- In Ouargla, the average high-temperature is 45 °C (113.1 °F) and the
average low-temperature, is 22.4 °C (72.3 °F). The average relative
humidity is 20.1% and during the entire year, the rain falls for
24 days and up to 40 mm (1.6″) of precipitation.
2.2. Sampling procedure
A cross-sectional study design was used. The camels followed up
were grouped according to their age and sex. A serological analysis was
performed to detect anti-T.gondii antibodies in the blood serum col­
lected. Since there was no previous expected prevalence in the area of
study, the sample size was determined according to Thrusfield (2005);
an expected prevalence of 50% was taken as a reference value since
there were no previous studies that could allow us to refer to a parti­
cular prevalence rate. A10% desired precision and a 95% confidence
level were considered.
Between January and March 2018, blood samples were collected
through the jugular from 320 dromedaries of both sexes, spread over 33
flocks whose 6 in Ouargla, 8 in El-Oued, 9 in Biskra and 10 in Ghadaia.
On average 9 animals per herd were randomly sampled. After blood
centrifugation the serum was stored at −20 °C until analysis.
Three age groups were set up: < 5 years, from 5 to 10 years and
˃10 years. Animals under 5 years are considered young, adults between
5 and 10 and of age and over 10 years as the older camels Additional
M.-C. Abdallah, et al. Veterinary Parasitology: Regional Studies and Reports 22 (2020) 100475

information concerning gender, breed, husbandry system (semi-in­
tensive or extensive), contact with others domestic animals, history of
abortion, source of water and geographic origin on all animals were
recorded.
2.3. Serological testing
Sera were tested for the presence of anti-T.gondii antibodies via an
ELISA test (ID Screen® Toxoplasmosis Indirect ELISA Multi-species,
ID.VET. Innovative Diagnostics. Montpellier, France) with a sensitivity
and specificity of 100% and 96% respectively, according to the man­
ufacturer's instructions and data. The technique used was that described
by Abdallah et al. (2019).
The results were expressed as optical density (OD); absorbance was
read at 450 nm (wave length) with an EL-800 ELISA Plate reader
(Biotek Instruments Inc., USA).
2.4. Statistical analysis
The data were inserted in an Excel file (Microsoft, 2016). All sta­
tistical analyses were performed using the statistical software SPSS
version 22.0 (SPSS Inc., Chicago, IL, USA).
Seroprevalence was calculated by dividing the number of animals
expressing anti-T.gondii antibodies by the total number of animals
tested. The relationship of risk factors with the dependent variables was
primarily assessed using cross tabulation.
Univariate regression analysis of fixed factors on T. gondii ser­
opositivity was carried out to determine those factors that explained
most variation in T. gondii seropositivity from the complete data set.
The multivariate logistic regression was obtained by using all variables
that showed a moderate statistical significance (p ˂ 0.05) in the uni­
variate analysis. The p value (p ˂ 0.05), odds ratio with 95% CI for
explanatory variables were also calculated.
3. Results
Out of 320 dromedaries surveyed for T. gondii antibodies, 48 (15%;
CI: 11.5–19.33) were seropositive by ELISA test.
The univariate analysis of risk factors at the individual-level in
dromedaries of southeastern Algeria (Table 1), showed that sex, breed,
contact with small ruminants, water source and history of abortion had
not significantly impacted T. gondii seropositivity (p > 0.05), whereas
age (p = 0.003), husbandry system (p = 0.012) and study area
(p = 0.000) represented real significant risk factors.
Individual seroprevalence was higher (P < 0.05) in camels > 5
years old (21.3%; CI: 15.1–27.5) than in those aged less than 2 years
(7.58%; CI: 1.19–13.97) and in camels living in intensive system
(26.15%; CI: 15.47–36.84) than in extensive one 10,8%; CI:
6.21–15.38). A statistically significant difference in seroprevalence was
observed between the studied geographical locations (region) with the
highest seroprevalence recorded in Biskra (29.57%; CI: 20.28–39.06)
and the lowest one in El-Oued (7.59%; CI: 1.75–13.44) as shown in
Fig. 1.
Three variables (age, husbandary system, and study area) that had a
p-value < 0.25 in the univariable analysis, were subjected to the mul­
tivariable regression model. The analysis showed a significant asso­
ciation between (1) T. gondii seropositivity and age (p = 0.003;
OR = 2.81; 95% CI: 1.51–3.45), (2) between T. gondii seropositivity
and region (p = 0.0001; OR = 3.91; 95% CI: 2.21–6.85) and between
T. gondii seropositivity and husbandry system (p = 0.001; OR = 2.5;
95% CI: 1.6–3.81) (Table 1).
The likelihood of T. gondii infection was two times higher in adult
dromedaries > 10 years old (OR = 2.81; CI: 1.51–3.87; p = 0.003),
two times higher in animals living in the intensive husbandry system
(OR = 2.42; CI: 1.3–3.07; p = 0.003), and four times higher in animals
living in Biskra (OR = 4.2; CI: 1.21–9.85; p = 0.0001) then Ouargla
(OR = 1.36; CI: 0.39–5.95), Ghardaia (OR = 1.29; CI: 0.23–7.44) and
El-Oued (Table 1).
4. Discussion
The present study reports for the first time evidence of T. gondii
infection together with its seroprevalence and risk factors in dromed­
aries in Algeria. An overall seroprevalence of 15% assessed via ELISA
was recorded. This indicates that T. gondii is widespread and circulates
among dromedaries in South-Eastern Algeria.
The seroprevalence rate obtained (15%) is higher than that recorded
in Iran (3.12%) (Dehkordi et al., 2013) and in Saudi Arabia (6.5%) (Al-
Anazi, 2011), but is more or less the same to that reported in Saudi
Arabia by Hussein et al. in 1988 (13.1%) (Hussein et al., 1988) and Al-
Anazi in 2012 (16%) (Al-Anazi, 2012). Higher seroprevalence was re­
ported in Sudan (20%) by Khalil and Elrayah in 2011, in the United

Table 1
Univariate and multivariate logistic regression analysis of factors influencing the risk of T. gondii seropositivity in dromedaries.
Univariate Multivariate

Variables N No. of positive Percentage (%) 95% CI P-value OR (95% CI) P-value

Age group (year) ˂5 66 5 7.58 1.2–13.97 0.003* Ref

5–10 85 7 8.23 2.4–14.1 1.08 (0.11–7.25) 0.003*
˃ 10 169 36 21.3 15.1–27.5 2.81 (1.51–3.87)
Gender Male 37 5 13.51 2.5–24.17
Female 283 43 15.19 11.01–19.38 0.9807
Breed Sahraoui 248 40 16.13 11.55–20.71
Tergui 72 8 11.11 3.85–18.37
Contact with sheep and goats Yes 119 24 20.17 12.96–27.38 0.067
No 201 24 11.94 7.46–16.42
Hasbandary system Extensive 176 19 10.8 6.21–15.38 0.012* Ref
Semi- Extensive 79 12 15.19 7.28–23.10 1.47 (0.4–6.33) 0.003*
Intensive 65 17 26.15 15.47–36.84 2.42 (1.3–3.67)
Water Source Well 229 33 14.41 9.86–18.96 0.768
Lakes 91 15 16.48 8.86–24.11
History of abortion Yes 87 16 18.4 10.3–26.5 0.388
No 233 32 13.73 9.13–18.15
Region (farm location) El-Oued 79 6 7.59 1.75–13.44 0.00007* Ref 0.0001*
Ghardaia 92 9 9.78 3.71–15.85 1.29 (0.23–7.44)
Ouargla 58 6 10.33 2.51–18.18 1.36 (0.39–5.98)
Biskra 91 27 29.57 20.28–39.06 4.21 (1,21 - 9,85)

N: number of animals tested; No.: number; CI: Confidence Interval; OR: odds ratio; *: significant.

3
M.-C. Abdallah, et al.
Arab Emirates (22.4%) by Abu-Zeid (2002) and in Egypt (from 17.4 to
31.4%) by Hilali et al., 1998 and Shaapan and Khalil (2008), respec­
tively.
The difference between the recorded seroprevalences can be due to
several factors, such as: (i) the sample size (Khalil and Elrayah, 2011);
(ii) serological testing limits and their difference in sensitivity (Al-
Anazi, 2011; Dubey, 2010); (iii) the density of cats and wild felines
(Gebremedhin et al., 2014.); (iv) stress, malnutrition and common
diseases such as trypanosomiasis (Kassa et al., 2011); (v) climatic
conditions and soil type (Dubey, 2010); (vi) the method and the prac­
tical management of livestock (Dubey and Jones, 2008; Gebremedhin
et al., 2014.).
Presence of T. gondii infection in camels suggests the potential
transmission of Toxoplasma infection to humans through consumption
of raw-undercooked meat or raw-insufficiently boiled milk from dro­
medaries.
When considering the low human population density as well as that
of domestic cats and the arid Saharan climate of the study area (South-
eastern Algeria) that is hostile to the oocysts' survival, the risk of ac­
quiring T. gondii oocysts is low. The seroprevalence obtained was to be
expected.
However, the presence of T. gondii infection in dromedaries in this
part of Algeria could be due to the migration of the camels to sub-arid
areas searching for better ranges where felids are usually more nu­
merous, the absence of regular culling programs and, poor veterinary
services. In addition, it could also be related to local ownership ex­
change and agricultural development (Megersa, 2010) and the cumu­
lative effects of camels to age (Tenter, 2009; Gebremedhin et al., 2014).
A positive correlation between seroreactivity and dromedaries age
(p = 0.0001) was shown in the present study. The seroprevalence of T.
gondii antibodies was seen to increase with age of the animals; this
supports the findings of other studies (Fahmy et al., 1979; Hussein
et al., 1988). It could be attributed to the longer exposure of adults
animals to the T. gondii infection since it was reported that animals that
live longer might be more likely to be exposed to different sources of T.
gondii parasites (Gebremedhin et al., 2014; Rouatbi et al., 2019).
There was no statistically significant sex-linked difference in ser­
oprevalence between males (13,51%; 95% CI: 2,5 - 24,53) and female's
dromedaries (15,19%; 95% CI: 11,01 -19,38). This is consistent with
what was found in dromedaries in Egypt (Fahmy et al., 1979), Saudi
Arabia (Hussein et al., 1988), Sudan (Elamin et al., 1992) and, in
bactrian camels (Camelus bactrianus) in China (Wang et al., 2013).
Regarding the husbandry system, significant difference was showed.
This result is in agreement with studies that identified intensive system
as a risk factor for T. gondii in camels in Ethiopia (Gebremedhin et al.,
2014). The transhumance by seasonal movement of livestock has pro­
found effect on the epidemiology and spread of this disease in south
Algeria.
Seropositivity varied between the areas investigated. Dromedaries
in Biskra (29.57%) are 3.91 times more likely to be seropositive than
camels of El-Oued (7.59%) [P < 0.0001]. This seroprevalence differ­
ence may be due to the variation in temperature and humidity in be­
tween the provinces of the study area. The environment was reported to
influence the epidemiology of toxoplasmosis (Yan et al., 2016). The
High Plains of Algeria like those on which Biskra lies have a very high
moisture content that increases the chances of oocyst's survival in the
environment. This can elevate the probability of contact with con­
taminated sources leading to higher seroprevalences (Jones et al., 2001;
Dubey, 2010; Tilahun et al., 2018). Humidity of the study area impact
the survival and epidemiological distribution of the parasite (Dubey,
2010; Tegegne et al., 2016).
In the current study, the “presence of cats” as a risk factor was not
investigated for this species was omnipresent. This may account for the
presence of T. gondii specific antibodies in the dromedaries tested as a
result of oocysts shedding of infected cats.
In conclusion, T. gondii infection of dromedary camels is widespread
4
Veterinary Parasitology: Regional Studies and Reports 22 (2020) 100475
in South-Eastern Algeria. Age, husbandry systems and geographical
study areas are independent predictors of T. gondii seropositivity. The
identification of risk factors is prerequisite to define the type of mea­
sures and strategies to be applied in order to lower, control and prevent
T. gondii infection in dromedary camels thereby reducing human in­
fection.
Declaration of Competing Interest
None.
Acknowledgements
The authors thank the Algerian Ministry of Higher Teaching and
Scientific Research for contributing to her PhD training.
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