The Seroprevalence of Ovine Toxoplasmosis in Fars Province, Southern Iran
This study determines the prevalence of ovine toxoplasmosis in Shiraz, Southern Iran. From April 2004 to May 2005, serum samples of 603 sheep were randomly collected in 18 Cities of Fars Province, Southern Iran and tested for toxoplasmosis using Indirect Fluorescent Antibody Technique (IFAT). The prevalence of toxoplasmosis was 26.5%, while the rate of seropositivities in 1/100, 1/200, 1/400 and 1/800 dilutions were 17.7, 2.8, 4.3 and 1.7%, respectively. The highest prevalence was in Abadeh (56.7%) and Nourabad (44.3%) cities and the lowest was determined Arsanjan (4.2%) whereas no infection was determined in Fasa. Considering the high prevalence of toxoplasmosis in sheep in our region, control measures need to be undertaken to prevent transmission of the infection to other animals and man by health and veterinary authorities. Therefore, it seems that standardization of techniques, hygienic standards in sheep breeding especially in cities with more migrating domestic animals and environmental health education for veterinary personnel are required to prevent human infection.
Toxoplasma gondii is a worldwide obligate intracellular protozoan parasite
in man and warm-blooded animals. Transmission to man happens by ingestion of
T. gondii oocysts shed into the environment by cats, or by consuming
meat of infected animals. Under normal immune conditions, T. gondii infection
is frequently asymptomatic, but in immunocompromised individuals, e.g., AIDS,
the parasites can become widely disseminated, resulting into severe toxoplasmosis
and encephalitis. Primary infections acquired during pregnancy may also cause
severe damages to the fetus, manifested as mental retardation, seizures, blindness
and death (Ajioka and Soldati, 2007). Toxoplasma gondii
is a protozoan that in man and animals can cause congenital abnormalities, abortion
(Smith and Reduck, 2000) death of fetus, chorioretinitis,
hydrocephaly, microcephaly and jaundice which leads to severe economical losses
(Joynson and Wreghitt, 2001). It has mild flu like symptoms
in immunocompetent humans, but the disease is severe in immunocompromised persons
such as HIV positive ones, 23% of which were reported to develop toxoplasmic
encephalitis (Oksenhendler et al., 1994). Using
Indirect Fluorescent Antibody Technique (IFAT), human seropositivity in Northern
and Southern parts of Iran was reported to be 55 and 29%, respectively with
a seroprevalence of 51.8% for all parts of Iran (Ghorbani
et al., 1978; Sedaghat et al., 1978;
Assmar et al., 1997). The disease occurs mostly
through ingestion of undercooked meat or by the oocyst excreted by an infected
cat as a definitive host (Dubey, 1998). Infected lambs
were reported as one of the most important sources of T. gondii worldwide
(Jacobs et al., 1960). The worldwide prevalence
of anti-T. gondii antibodies in sheep was reported up to 89% (Tenter
et al., 2000). Since, sheep breeding is the most common source of
meat in Fars Province, Southern Iran and considering that infected lambs can
be sources of human infection and due to economic losses of ovine abortion and
the public importance of the disease, this study was performed to determine
the prevalence of T. gondii among sheep in Southern Iran.
MATERIALS AND METHODS
During 2004-2005 using a cluster random sampling method, a total of 603 blood
samples were provided from reared sheep in 18 cities of Fars Province in Southern
Iran Fig. 1. The IFAT cut off point for T. gondii was
considered as 1:100 diluted in PBS (0.1 M phosphate, 0.33 M NaCl, pH = 7.2)
for preliminary screening (Esteban-Redondo et al.,
1999). The positive samples were serially diluted up to 1:800 to obtain
the real titer of IgG antibody. RH strain tachyzoite of T. gondii was
used as antigen (Pasteur Institute, Tehran, Iran) to be fixed on wells of immunofluorescent
||A sketch map of Iran, showing the location of towns in Fars
Province, Southern Iran
Ten microliters of each diluted serum was placed on each well and incubated
in a humidified chamber at 37°C for 30 min. Slides were washed in PBS (two
times, 7 min), dried and then were incubated for 30 min at 37°C with rabbit
anti-sheep IgG conjugate (Bethyl Co.), diluted 1:250 in PBS. Evans Blue also
diluted 1:10000 in this solution. Slides were washed and air-dried. A drop of
glycerol buffer was added on to each slide and then was covered with a cover-slip.
Finally, the samples were observed under the immunofluorescent microscope (Zeiss,
HBO 50). The results were analyzed by SPSS software using Chi-square test and
a p-value <0.05 was considered statistically significant.
RESULTS AND DISCUSSION
The prevalence of toxoplasmosis in sheep in Southern Iran was 26.5%. In titers of 1:100, 1:200, 1:400 and 1:800, 17.7, 2.8, 4.3 and 1.7% were positive for infection, respectively (Table 1). The rate of infection from 18 cities was shown in Table 2: the highest prevalence was in Abadeh (56.7%, p = 0.01) and Nourabad (44.3%, p = 0.01) cities and the lowest was determined Arsanjan (4.2%) whereas no infection was determined in Fasa.
The sources of infection for humans worldwide greatly vary with differences
in culture, ethnicity, geographical region and food habits. Food animals such
as pigs, sheep and goats have a higher frequency of tissue cysts compared to
other animals (Tenter et al., 2000). Present
study demonstrated a seroprevalence of 26.5% in sheep that is close to results
of some studies from Spain, Italy and Morocco (28.4, 23.1 and 27.6%, respectively)
(Masala et al., 2003; Pereira-Bueno
et al., 2004; Sawadogo et al., 2005).
Also, the prevalence was markedly high in humid regions such as France (Cabannes
et al., 1997), Serbia (Klun et al., 2006)
and Austria (Edelhofer and AspÖck, 1996) as the
rates were 92, 84.5 and 66%, respectively. The prevalence in Turkey (Altinas
et al., 1997), Saudi Arabia (El-Metenawy, 2000)
and Pakistan (Zaki, 1995) as our neighbor countries
were 40, 3 and 3%, respectively.
||The titers of toxoplasmosis in sheep in Southern Iran
||The rate of toxoplasmosis infection in sheep in Southern Iran
Furthermore, the rate of infection from other parts of Iran was reported 24.5%
(Hashemi-Fesharki, 1996), 25.5% in Central Iran (Chegini
et al., 1999) and 14% in South Western parts of the country (Hoghooghi-Rad
and Afraa, 1993). Several factors such as management and hygienic standards
in breeding livestock, density of cats and environmental conditions are effective
on the acquisition of T. gondii oocysts (Tenter et
al., 2000). Humidity and temperate favor the oocyst survival. Moreover,
the high levels of congenital transmission and potential survival of infected
lambs in sheep were demonstrated previously (Duncanson et
al., 2001), suggesting that vertical transmission may play an important
role in maintenance of the parasite in natural populations of sheep without
requiring for ingestion of oocysts excreted by cats. Fars Province in Southern
Iran is characterized by dry weather and sub-Saharan environment and an average
annual rainfall not over than 350 mm. However, other characters such as temperature
and altitude in these areas have wide range. The majority of sheep in Fars Province
are raised by migrating nomads that move to distant summer and winter quarters
(more than 600 km away) in search of food for their animals. Abadeh in Northern
areas and Nourabad in Southern localities with the highest prevalence have the
highest nomadic population and Fasa in eastern parts and Arsanjan in Western
regions with the lowest prevalence have the lowest nomadic population that explains
the difference. Based on cultural and food habits in this area, tissue cysts
of T. gondii in meat and viscera of sheep must be considered important
sources of infection in human. Masala et al. (2003)
indicated that T. gondii infection plays an important role in ovine abortion
in Italy and livestock toxoplasmosis should be economically considered important
(Masala et al., 2003). This fact explains 4.7
billions $ loss due to sheep abortion in Uruguay (Freyre
et al., 1997).
Therefore, standardization of techniques, hygienic standards in sheep breeding especially in cities with more migrating domestic animals and environmental health education for veterinary personnel are required to prevent human infection.
The authors would like to thank Shiraz University of Medical Sciences for financial support and the Center for Development of Clinical Studies of Shiraz University of Medical Sciences for typing of manuscript.
1: Altinas, K., C. Gungor, H. Zeybek and C. Yarali, 1997. Sabin-Feldman testi ile Ankara yoresi koyunlarinda Toxoplasma gondii prevalensinin saptanmasi. Turk. Parazitol. Derg., 21: 63-65.
2: Assmar, M., A. Amirkhani, N. Piazak, A. Hovaesian, A. Koolobandi and R. Etessami, 1997. Toxoplasmosis in Iran. Results of a seroepidemiological study. Bull. Soc. Pathol. Exot., 90: 19-21.
3: Cabannes, A., F. Lucchese and J.C. Hernandez, 1997. Enquete seroepidemiologique sur Toxoplasma gondii chez les ovins, bovins et felins dans le department de la Gironde. Bull. Soc. France Parasitol., 15: 11-22.
4: Chegini, S., M. Asmar, A.R. Abadi and S.A. Bagheri Yazdi, 1999. Toxoplasma infection in human and domestic animals. J. Babol. Univ Med. Sci., 12: 47-52.
5: Dubey, J.P., 1998. Advances in the life cycle of Toxoplasma gondii. Int. J. Parasitol., 28: 1019-1024.
CrossRef | Direct Link |
6: Duncanson, P., R.S. Terry, J.E. Smith and G. Hide, 2001. High levels of congenital transmission of Toxoplasma gondii in a commercial sheep flock. Int. J. Parasitol., 31: 1699-1703.
7: Edelhofer, R. and H. Aspock, 1996. Infektionsquellen und infectionswege aus der sicht des toxoplasmose-screening der schwangeren in ֖sterreich. Mitt. ֖sterrGes. Tropenemed. Parasitol., 18: 59-70.
8: El-Metenawy, T.M., 2000. Seroprevalece of Toxoplasma gondii antibodies among domesticated ruminants at Al-Qassim region, Saudi Arabia. Dtsch. Tieraztl. Wochenschr., 107: 32-33.
9: Esteban-Redondo, I., S.W. Maley, K. Thomson, S. Nicoll, S. Wright, D. Buxton and E.A. Innes, 1999. Detection of T. gondii in tissues of sheep and cattle following oral infection. Vet. Parasitol., 86: 155-171.
CrossRef | Direct Link |
10: Freyre, A., J. Bononino, D. Falcon, O. Castells, A. Correa and J. Casaretto, 1997. The incidence and economic significance of ovine toxoplasmosis in Uruguay. Vet. Parasitol., 73: 13-15.
11: Ghorbani, M., G.H. Edrissian and N. Assad, 1978. Serological survey of toxoplasmosis in the Northern part of Iran, using indirect fluorescent antibody technique. Trans. R. Soc. Trop. Med. Hyg., 72: 369-371.
12: Hashemi-Fesharki, R., 1996. Seroprevalence of Toxoplasma gondii in cattle, sheep and goats in Iran. Vet. Parasitol., 61: 1-3.
13: Hoghooghi-Rad, N. and M. Afraa, 1993. Prevalence of Toxoplasmosis in humans and domestitic animals in Ahwaz, Capital of Khoozestan Province, South-West Iran. J. Trop. Med. Hyg., 96: 163-168.
14: Jacobs, L., J.S. Remington and M.L. Melton, 1960. A survey of meat samples from swine, cattle and sheep for the presence of encysted toxoplasma. J. Parasitol., 46: 23-28.
15: Joynson, D.H.M. and T. Wreghitt, 2001. Toxoplasmosis: A Comprehensive Clinical Guide. Cambridge University Press, Cambridge, pp: 193-276.
16: Klun, I., O. Djurkovic-Djakovic, S. Katic-Radivojevic and A. Nikolic, 2006. Cross-sectional survey on Toxoplasma gondii infection in cattle, sheep and pigs in Serbia: Seroprevalence and risk factors. Vet. Parasitol., 135: 121-131.
17: Masala, G., R. Porcu, L. Madau, A. Tanda and B. Ibba, G. Satta and S. Tola, 2003. Survey of ovine and caprine toxoplasmosis by IFAT and PCR assays in Sardinia, Italy. Vet. Parasitol., 117: 15-21.
18: Oksenhendler, E., I. Charreau, C. Tournerie, M. Azihary, C. Carbon and J.P. Aboulker, 1994. Toxoplsma gondii infection in advanced HIV-infection. J. Acquir. Immunol. Defic. Syndr., 8: 483-487.
19: Pereira-Bueno, J., A. Quintanilla-Gozalo, V. Perez-Perez, G. Alvarez-Garcia, E. Collantes-Fernandez and L.M. Ortega-Mora, 2004. Evaluation of ovine abortion associated with Toxoplasma gondii in Spain by different diagnostic techniques. Vet. Parasitol., 121: 33-43.
20: Sedaghat, A., S.M. Ardehali, M. Sadigh and M. Buxton, 1978. The prevalence of toxoplasmosis infection in Southern Iran. J. Trop. Med. Hyg., 81: 204-207.
21: Sawadogo, P., J. Hafid, B. Bellete, R.T. Sung and M. Chakdi et al., 2005. Seroprevalence of T. gondii in sheep from Marrakech, Morocco. Vet. Parasitol., 131: 89-92.
22: Smith, J.E. and N.R. Reduck, 2000. Toxoplasma Gondii Strain Variation and Pathogenicity. In: Microbial Foodborne Diseases: Mechanisms of Pathogenesis and Toxin Synthesis, Cary, J.W., J.E. Linz and B. Bhatnaga (Eds.). Technnomic Publishing, Lancaster.
23: Tenter, A.M., A.R. Heckeroth and L.M. Weiss, 2000. Toxoplasma gondii: From animals to humans. Int. J. Parasitol., 30: 1217-1258.
CrossRef | PubMed | Direct Link |
24: Zaki, M., 1995. Seroprevalence of Toxoplasma gondii in domestic animals in Pakistan. J. Pak. Med. Assoc., 45: 4-5.
25: Ajioka, J.W. and D. Soldati, 2007. Toxoplasma: Molecular and Cellular Biology. Horizon Bioscience, Norfolk, UK., ISBN: 978-1-904933-34-2, pp: 37-58.