**1. Introduction**

36 Toxoplasmosis – Recent Advances

microbiol. 43: 475-481.

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detection in water. Appl. environ. microbiol. 70: 4035–4039.

[183] Dubey JP, Hill DE, Rozeboom DW, Rajendran C, Choudhary S, Ferreira LR, Kwok OC, Su C (2012) High prevalence and genotypes of *Toxoplasma gondii* isolated from organic

[184] Kijlstra A, Jongert E (2009) Toxoplasma-safe meat: close to reality? Trends parasitol. 25:

[185] Lélu M, Gilot-Fromont E, Aubert D, Afonso E, Dupuis E, Gotteland C, Dardé ML, Marnef F, Poulle ML, Richaume-Jolion A, Villena I (2011) Development of a sensitive method for *Toxoplasma gondii* oocysts extraction in soil samples. Vet. parasitol. 183: 59-

[186] Villena I, Aubert D, Gomis P, Ferté H, Inglard JC, Denis-Bisiaux H, Dondon JM, Pisano E, Ortis N, Pinon JM (2004) Evaluation of a strategy for *Toxoplasma gondii* oocyst

[187] Kourenti C, Karanis P (2006) Evaluation and applicability of a purification method coupled with nested PCR for the detection of *Toxoplasma* oocysts in water. Lett. appl.

[188] Borchardt MA, Spencer SK, Bertz PD, Ware MW, Dubey JP, Alan Lindquist HD (2009) Concentrating *Toxoplasma gondii* and *Cyclospora cayetanensis* from surface water and drinking water by continuous separation channel centrifugation. J. appl. microbiol. 107:

[189] Du F, Zhanga Q, Yu Q, Hu M, Zhou Y, Zhao J (2012) Soil contamination of Toxoplasma gondii oocysts in pig farms in central China. Vet. parasitol.

[190] Hill D, Coss C, Dubey JP, Wroblewski K, Sautter M, Hosten T, Muñoz-Zanzi C, Mui E, Withers S, Boyer K, Hermes G, Coyne J, Jagdis F, Burnett A, McLeod P, Morton H, Robinson D, McLeod R (2011) Identification of a sporozoite-specific antigen from

[191] Muñoz-Zanzi CA, Fry, P Lesina B, Hill D (2010) *Toxoplasma gondii* Oocyst–specific

[192] Muñoz-Zanzi C, Tamayo R, Balboa J, Hill D (2012) Detection of oocyst-associated toxoplasmosis in swine from Southern Chile. Zoonoses pub. health. doi: 10.1111/j.1863-

[193] Boyer K, Hill D, Mui E, Wroblewski K, Karrison T, Dubey JP, Sautter M, Noble AG, Withers S, Swisher C, Heydemann P, Hosten T, Babiarz J, Lee D, Meier P, McLeod R (2011) Toxoplasmosis Study Group. Unrecognized ingestion of *Toxoplasma gondii* oocysts leads to congenital toxoplasmosis and causes epidemics in North America. Clin.

Antibodies and Source of Infection. Emerg. infect. dis 16: 1591-1596.

Toxoplasmosis is a globally distributed parasitic zoonosis. Cats and other *Felidae* are the definitive host of the *Toxoplasma gondii* parasite, in whose intestines the sexual cycle takes place, and they are the primary source of infection to all animals including humans, by way of contaminating the environment with oocysts excreted in the feces (Dubey, 2010). Herbivores are infected by ingestion of food and water contaminated by oocysts, and carnivores by eating tissue cysts present in the flesh of infected animals. Omnivores including humans are infected by both routes – by oocysts via improperly washed vegetables or fruits, contaminated water or hands, and by tissue cysts via improperly processed or raw meat. Vertical transmission, from mother to offspring, may occur, and is the cause of congenital toxoplasmosis (CT). CT is actually the major *T. gondii*-induced clinical entity, which, along with opportunistic infection in immunocompromised patients, defines the clinical significance of toxoplasmosis. The gravity of the potential consequences of CT on the one hand, and the preventability of the disease on the other, call for implementation of prevention programs. A prerequisite for an adequate choice of prevention strategy is continuous monitoring of the local epidemiological situation.

This chapter reviews the epidemiology and epizootiology of *T. gondii* infection in South-East Europe (SEE). SEE is here considered as the territory comprising the Balkan Peninsula (35° – 46°53' N latitude, 13°23' – 30° E longitude), bordered by the Adriatic Sea to the west, the Mediterranean Sea to the south, the Black Sea to the east and the rivers Sava and Danube to the north, encompassing the countries descending from ex-Yugoslavia including Slovenia, Croatia, Bosnia & Herzegovina, Serbia, Montenegro and FYR of Macedonia (FYRoM), as well as Albania, Bulgaria and mainland Greece. Most of the area is mountainous, while the climate varies from Mediterranean to moderate. The whole region has a combined area of 550,000 km2 and a population of 55 million.

© 2012 Bobić et al., licensee InTech. This is an open access chapter distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. © 2012 The Author(s). Licensee InTech. This chapter is distributed under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

## **2. Epidemiology of toxoplasmosis in SEE**

We analysed epidemiological data published in the last 20 years for all SEE countries except Bulgaria and Bosnia & Herzegovina for which none were available. Data in the published reports were obtained using a wide array of immunodiagnostic assays which may somewhat limit comparisons. Indeed, the tests in use have varied over time both among and within individual countries, and included the Sabin-Feldman test (SFT), complement fixation test (CFT), indirect fluorescence (IFAT) to direct agglutination (DA) and ELISA, whether in-house or commercial; the latter ones were obtained from various manufacturers. However, this limitation applies to any such review (Gilbert & Peckham, 2002), and moreover, the pattern of infection observed in the region despite the variety of tests with their different specificities, sensitivities, cut-offs etc., rather emphasizes the described trends.

*Toxoplasma gondii* Infection in South-East Europe: Epidemiology and Epizootiology 39

**Figure 1.** Prevalence of *Toxoplasma gondii* infection in generative age women in South-East Europe

of undercooked meat was not found to be a risk factor.

to such a change, including increased public awareness as a result of health education, better hygiene on livestock farms, and more frequent use of frozen meat. However, according to the SEE data, the listed factors seem not to be exhaustive; although better farming conditions along with the increased consumption of frozen meat (freezers now present in most households) may have contributed to a decrease in the infection prevalence in Serbia and Albania, a decreasing trend was also noted in FYRoM and Greece where consumption

It appears that, according to reports from the eastern part of the region, there is a north-tosouth decrease in the infection prevalence (Table 1). For instance, in 1994, the prevalence ranged from 69% in southern Hungary (as a region neighbouring the SEE to the north) (Szénási et al., 1997), over 53% in Serbia (Bobić et al., 2003) to 26% in northern Greece (Diza et al., 2005). This trend was also evident within SEE in all years for which comparative data were available (2002: Serbia 36%, FYRoM 25%; 2004: Serbia 32%, Northern Greece 20%; 2007: Serbia 31%, Northern Greece 21%) (Cvetković et al., 2003; Diza et al., 2005; Bobić et al., 2007; Kansouzidou et al., 2008; Bobić et al., 2011). Moreover, a significant north-to-south decrease in the infection prevalence was also shown within Serbia itself (Bobić et al., 2003). The northto-south decrease in the prevalence of infection within SEE suggests a possible influence of climatic conditions, which vary across the region from continental to Mediterranean, and

countries (1984-2009)

over time as well.

The vast majority of epidemiological data on toxoplasmosis in SEE comes from studies in women of generative age, and a few from studies in immunocompromised patients.

#### **2.1. Toxoplasmosis in generative age women**

Data on the prevalence of *T. gondii* infection in SEE countries are presented in Figure 1. In the last ten years, the prevalence has not surpassed 50% anywhere in the region, ranging from 20% in Greece (Diza et al., 2005) to 49% in Albania (Maggi et al., 2009). Wide differences in the prevalence of infection are generally characteristic of Europe, since the infection prevalence is currently ranging from 8.2% in Switzerland (Lausanne and Geneva) (Zufferey et al., 2007) to 57.6% in Timisoara-Romania (Olariu et al., 2008). Differences in the prevalence of *T. gondii* infection are commonly explained by differences in life-style habits pertaining to risk factors for transmission in particular milieus. Not many studies on infection risk factors have been published in SEE countries, but those available identified consumption of undercooked meat as the leading risk factor for transmission in Serbia and, more recently, in Albania (Bobić et al., 1998; 2003; 2007; Maggi et al., 2009), and contact with soil in northern Greece and FYRoM (Decavalas et al., 1990; Diza et al., 2005; Cvetković et al., 2010). Exposure to soil was also considered to account for the higher prevalence of infection in rural *vs.* urban women in Croatia.

Continuous monitoring of the prevalence of *T. gondii* infection in women of childbearing age in Slovenia, Serbia and Greece has showed a significant decrease in the infection prevalence since the eighties onwards. The largest decrease, from 86% in 1988 to 31% in 2007 (Bobić et al., 2003; 2007), was noted in Serbia. Furthermore, a trend of decreasing prevalence has been shown during the last decade in FYRoM, from 25% in 2002 to 20% in 2005 (Cvetković et al., 2003; 2010) and in Montenegro, a rather dramatic one, from 41% in 2001 to 27% in 2007 (Mišković et al., 2003; Rajković & Vratnica, 2008). These data suggest that a decrease in the prevalence is a region-wide feature (Fig. 1).

A decreasing trend of *T. gondii* infection prevalence noted in the SEE region is obviously part of a Europe-wide changing pattern of *T. gondii* infection over the last 30 years (Aspöck & Pollak, 1992; Nowakowska et al., 2006; Berger et al., 2009). Many factors have contributed

**2. Epidemiology of toxoplasmosis in SEE** 

**2.1. Toxoplasmosis in generative age women** 

in rural *vs.* urban women in Croatia.

prevalence is a region-wide feature (Fig. 1).

We analysed epidemiological data published in the last 20 years for all SEE countries except Bulgaria and Bosnia & Herzegovina for which none were available. Data in the published reports were obtained using a wide array of immunodiagnostic assays which may somewhat limit comparisons. Indeed, the tests in use have varied over time both among and within individual countries, and included the Sabin-Feldman test (SFT), complement fixation test (CFT), indirect fluorescence (IFAT) to direct agglutination (DA) and ELISA, whether in-house or commercial; the latter ones were obtained from various manufacturers. However, this limitation applies to any such review (Gilbert & Peckham, 2002), and moreover, the pattern of infection observed in the region despite the variety of tests with their different specificities, sensitivities, cut-offs etc., rather emphasizes the described trends. The vast majority of epidemiological data on toxoplasmosis in SEE comes from studies in

women of generative age, and a few from studies in immunocompromised patients.

Data on the prevalence of *T. gondii* infection in SEE countries are presented in Figure 1. In the last ten years, the prevalence has not surpassed 50% anywhere in the region, ranging from 20% in Greece (Diza et al., 2005) to 49% in Albania (Maggi et al., 2009). Wide differences in the prevalence of infection are generally characteristic of Europe, since the infection prevalence is currently ranging from 8.2% in Switzerland (Lausanne and Geneva) (Zufferey et al., 2007) to 57.6% in Timisoara-Romania (Olariu et al., 2008). Differences in the prevalence of *T. gondii* infection are commonly explained by differences in life-style habits pertaining to risk factors for transmission in particular milieus. Not many studies on infection risk factors have been published in SEE countries, but those available identified consumption of undercooked meat as the leading risk factor for transmission in Serbia and, more recently, in Albania (Bobić et al., 1998; 2003; 2007; Maggi et al., 2009), and contact with soil in northern Greece and FYRoM (Decavalas et al., 1990; Diza et al., 2005; Cvetković et al., 2010). Exposure to soil was also considered to account for the higher prevalence of infection

Continuous monitoring of the prevalence of *T. gondii* infection in women of childbearing age in Slovenia, Serbia and Greece has showed a significant decrease in the infection prevalence since the eighties onwards. The largest decrease, from 86% in 1988 to 31% in 2007 (Bobić et al., 2003; 2007), was noted in Serbia. Furthermore, a trend of decreasing prevalence has been shown during the last decade in FYRoM, from 25% in 2002 to 20% in 2005 (Cvetković et al., 2003; 2010) and in Montenegro, a rather dramatic one, from 41% in 2001 to 27% in 2007 (Mišković et al., 2003; Rajković & Vratnica, 2008). These data suggest that a decrease in the

A decreasing trend of *T. gondii* infection prevalence noted in the SEE region is obviously part of a Europe-wide changing pattern of *T. gondii* infection over the last 30 years (Aspöck & Pollak, 1992; Nowakowska et al., 2006; Berger et al., 2009). Many factors have contributed

**Figure 1.** Prevalence of *Toxoplasma gondii* infection in generative age women in South-East Europe countries (1984-2009)

to such a change, including increased public awareness as a result of health education, better hygiene on livestock farms, and more frequent use of frozen meat. However, according to the SEE data, the listed factors seem not to be exhaustive; although better farming conditions along with the increased consumption of frozen meat (freezers now present in most households) may have contributed to a decrease in the infection prevalence in Serbia and Albania, a decreasing trend was also noted in FYRoM and Greece where consumption of undercooked meat was not found to be a risk factor.

It appears that, according to reports from the eastern part of the region, there is a north-tosouth decrease in the infection prevalence (Table 1). For instance, in 1994, the prevalence ranged from 69% in southern Hungary (as a region neighbouring the SEE to the north) (Szénási et al., 1997), over 53% in Serbia (Bobić et al., 2003) to 26% in northern Greece (Diza et al., 2005). This trend was also evident within SEE in all years for which comparative data were available (2002: Serbia 36%, FYRoM 25%; 2004: Serbia 32%, Northern Greece 20%; 2007: Serbia 31%, Northern Greece 21%) (Cvetković et al., 2003; Diza et al., 2005; Bobić et al., 2007; Kansouzidou et al., 2008; Bobić et al., 2011). Moreover, a significant north-to-south decrease in the infection prevalence was also shown within Serbia itself (Bobić et al., 2003). The northto-south decrease in the prevalence of infection within SEE suggests a possible influence of climatic conditions, which vary across the region from continental to Mediterranean, and over time as well.


*Toxoplasma gondii* Infection in South-East Europe: Epidemiology and Epizootiology 41

Toxoplasmosis is a major opportunistic infection causing life-threatening disease in immunocompromised individuals, which is considered to be a consequence of reactivation of previously latent infection. Although opportunistic infection due to *T. gondii* has long been known in organ/tissue transplantations and patients with malign or systemic diseases on treatment with immunosuppressive effect, data on toxoplasmosis in the immunocompromised population in SEE are available only from groups of HIV-infected individuals and even these are scarce. In Serbia, out of a cohort of 339 patients diagnosed with AIDS during a five year period (1991-95), 288 were tested for *T. gondii* infection and the prevalence was 44.1% (Djurković-Djaković et al., 1997). A more recent Croatian study of 219 blood donors and 166 HIV-infected patients referred to the Zagreb University Hospital for Infectious Diseases "Dr. Fran Mihaljević" in 2000-2001, the seroprevalence of toxoplasmosis was 52.5% and 51.8%, respectively (Đaković-Rode et al., 2010), confirming that the prevalence of *T. gondii* infection among HIV-positive individuals is similar to that in the general population. Interestingly, whereas the risk for developing TE was not associated with age, sex or HIV transmission risk factor in Serbia (Djurković-Djaković et al., 1997), the Croatian study established a higher risk of *T. gondii* infection (OR 2.37) for men who have sex with men (Đaković-Rode et al., 2010). In the Serbian study, of the 288 examined HIV-infected patients, 31 developed toxoplasmic encephalitis, indicating an overall attack rate of 7.8%. At the time, the cumulative incidence of toxoplasmic encephalitis in *T. gondii*-seropositive patients was estimated at 32.7% for 60 months. However, the subsequent wide use of highly active antiretroviral treatment has allowed for good control of formerly AIDS-defining opportunistic infections including

Although the population structure of *T. gondii* isolates throughout the world is currently a major research interest in the field of toxoplasmosis (Ajzenberg et al. 2002; Sibley et al., 2009), such studies are at its beginning in SEE. As concerns the data on *T. gondii* genotypes present in the SEE region, there is a single published report of a type II strain genotype isolated from a case of congenital toxoplasmosis in Serbia (Djurković-Djaković et al. 2006). Current data on this issue in Serbia are reported elsewhere in this book (Ivović et al.). It is to be hoped that with the increased use of molecular methodologies in the region, work will be

Strategies for the prevention of CT include general screening-in-pregnancy programs and health education, and countries with a low prevalence of infection generally opt for health education (Kravetz et Federman, 2005; Gilbert and Peckham, 2002), while those with a high prevalence adopt screening-in-pregnancy programs (Aspöck & Pollak, 1992; Thulliez, 1992). In the SEE, a systematic program for the prevention of CT based on serological screening of pregnant women and health education has been implemented in Slovenia, while no other country has a systematic prevention program (Logar et al, 2002). The changing pattern of

performed which will contribute to the pan-European map of *T. gondii* genotypes.

**2.2. Toxoplasmosis in immunocompromised patients** 

toxoplasmosis, significantly decreasing their significance.

**2.3. Molecular epidemiology** 

**2.4. Prevention of human toxoplasmosis** 

1) Szénási et al., 1997; 2) Bobić et al., 1997; 3) Bobić et al., 2007; 4) Cvetković et al., 2003; 5) Cvetković et al., 2010; 6) Diza et al., 2005; 7) Kansouzidou et al., 2008; 8) Bobić et al., 2011

**Table 1.** Decrease of prevalence of *Toxoplasma gondii* infection from North to South in three SEE countries

Seasonality of infection was examined in Slovenia (Logar et al., 2005) in the west and Serbia (Bobić et al., 2010) in the east. Both studies showed a strong seasonality, with significantly more cases of acute infection in the winter than in the summer months (Fig. 2). In Slovenia, seasonality of infection was attributed to "more frequent and closer contacts with potentially *T. gondii* infected cats, which prefer to stay indoors during this period" (Logar et al., 2005). In contrast, more cases of acute infection in the winter in Serbia were explained by a higher influence of undercooked meat consumption in the winter period (Bobić et al., 2010).

**Figure 2.** Seasonality of *Toxoplasma gondii* infection in Slovenia (1999-2004) and Serbia (2004-2008) (Logar et al., 2005; Bobić et al., 2010)

Accordingly, the decrease in the prevalence of *T. gondii* infection in the SEE seems independent of the varying influence of risk factors for infection transmission throughout the region. However, this may prove not to be entirely true, as the above analysis was based on the limited data reported, which were often not acquired through systematic nation-wide research, and which were mainly derived from epidemiological questionnaires of variable precision level. For an accurate insight into the risk factors of major significance for human *T. gondii* infection, more research, based on larger patient series and carried out in different SEE areas, including case-control studies, would be preferable.

#### **2.2. Toxoplasmosis in immunocompromised patients**

40 Toxoplasmosis – Recent Advances

1991 73% (1) 69% (2) 1992 70% (1) 75% (2) 1993 64% (1) 58% (2)

et al., 2005; 7) Kansouzidou et al., 2008; 8) Bobić et al., 2011

(Logar et al., 2005; Bobić et al., 2010)

**Year South Hungary Serbia FYR Macedonia Northern Greece**

1994 69% (1) 53% (2) 26% (6)

2004 32% (3) 20% (5) 20% (6) 2007 31% (8) 21% (7) 1) Szénási et al., 1997; 2) Bobić et al., 1997; 3) Bobić et al., 2007; 4) Cvetković et al., 2003; 5) Cvetković et al., 2010; 6) Diza

**Table 1.** Decrease of prevalence of *Toxoplasma gondii* infection from North to South in three SEE countries

Seasonality of infection was examined in Slovenia (Logar et al., 2005) in the west and Serbia (Bobić et al., 2010) in the east. Both studies showed a strong seasonality, with significantly more cases of acute infection in the winter than in the summer months (Fig. 2). In Slovenia, seasonality of infection was attributed to "more frequent and closer contacts with potentially *T. gondii* infected cats, which prefer to stay indoors during this period" (Logar et al., 2005). In contrast, more cases of acute infection in the winter in Serbia were explained by a higher

influence of undercooked meat consumption in the winter period (Bobić et al., 2010).

**Figure 2.** Seasonality of *Toxoplasma gondii* infection in Slovenia (1999-2004) and Serbia (2004-2008)

SEE areas, including case-control studies, would be preferable.

Accordingly, the decrease in the prevalence of *T. gondii* infection in the SEE seems independent of the varying influence of risk factors for infection transmission throughout the region. However, this may prove not to be entirely true, as the above analysis was based on the limited data reported, which were often not acquired through systematic nation-wide research, and which were mainly derived from epidemiological questionnaires of variable precision level. For an accurate insight into the risk factors of major significance for human *T. gondii* infection, more research, based on larger patient series and carried out in different

2002 36% (3) 25% (4)

Toxoplasmosis is a major opportunistic infection causing life-threatening disease in immunocompromised individuals, which is considered to be a consequence of reactivation of previously latent infection. Although opportunistic infection due to *T. gondii* has long been known in organ/tissue transplantations and patients with malign or systemic diseases on treatment with immunosuppressive effect, data on toxoplasmosis in the immunocompromised population in SEE are available only from groups of HIV-infected individuals and even these are scarce. In Serbia, out of a cohort of 339 patients diagnosed with AIDS during a five year period (1991-95), 288 were tested for *T. gondii* infection and the prevalence was 44.1% (Djurković-Djaković et al., 1997). A more recent Croatian study of 219 blood donors and 166 HIV-infected patients referred to the Zagreb University Hospital for Infectious Diseases "Dr. Fran Mihaljević" in 2000-2001, the seroprevalence of toxoplasmosis was 52.5% and 51.8%, respectively (Đaković-Rode et al., 2010), confirming that the prevalence of *T. gondii* infection among HIV-positive individuals is similar to that in the general population. Interestingly, whereas the risk for developing TE was not associated with age, sex or HIV transmission risk factor in Serbia (Djurković-Djaković et al., 1997), the Croatian study established a higher risk of *T. gondii* infection (OR 2.37) for men who have sex with men (Đaković-Rode et al., 2010). In the Serbian study, of the 288 examined HIV-infected patients, 31 developed toxoplasmic encephalitis, indicating an overall attack rate of 7.8%. At the time, the cumulative incidence of toxoplasmic encephalitis in *T. gondii*-seropositive patients was estimated at 32.7% for 60 months. However, the subsequent wide use of highly active antiretroviral treatment has allowed for good control of formerly AIDS-defining opportunistic infections including toxoplasmosis, significantly decreasing their significance.

#### **2.3. Molecular epidemiology**

Although the population structure of *T. gondii* isolates throughout the world is currently a major research interest in the field of toxoplasmosis (Ajzenberg et al. 2002; Sibley et al., 2009), such studies are at its beginning in SEE. As concerns the data on *T. gondii* genotypes present in the SEE region, there is a single published report of a type II strain genotype isolated from a case of congenital toxoplasmosis in Serbia (Djurković-Djaković et al. 2006). Current data on this issue in Serbia are reported elsewhere in this book (Ivović et al.). It is to be hoped that with the increased use of molecular methodologies in the region, work will be performed which will contribute to the pan-European map of *T. gondii* genotypes.

#### **2.4. Prevention of human toxoplasmosis**

Strategies for the prevention of CT include general screening-in-pregnancy programs and health education, and countries with a low prevalence of infection generally opt for health education (Kravetz et Federman, 2005; Gilbert and Peckham, 2002), while those with a high prevalence adopt screening-in-pregnancy programs (Aspöck & Pollak, 1992; Thulliez, 1992). In the SEE, a systematic program for the prevention of CT based on serological screening of pregnant women and health education has been implemented in Slovenia, while no other country has a systematic prevention program (Logar et al, 2002). The changing pattern of

infection across the region currently complicates the choice of prevention strategy. A decrease in the prevalence of infection in women of childbearing age implies a rising proportion of women susceptible to infection in pregnancy, which, in turn, may lead to an increase in the incidence of congenital infections. Indeed, an increase in the incidence of primary infections in pregnancy has been shown through systematic screening-in-pregnancy programs; in Austria, which has been screening all pregnant women ever since 1975, the decrease in *T. gondii* prevalence from 50% to 37% during the 1980s was followed by an increase in the incidence of primary infections in pregnancy from 0.4% to 0.8% (Aspöck & Pollak, 1992). Similarly, in Slovenia, the decrease in the prevalence of infection from the early 1980s onwards, therefore before the introduction of the systematic prevention program in 1995, has been associated with an increased incidence of infections in pregnancy from 0.33% in the early 1980s to 0.75% in the early 1990s and to 0.94% in the late 1990s (Logar et al., 1995; 2002).

*Toxoplasma gondii* Infection in South-East Europe: Epidemiology and Epizootiology 43

but did not perform genetic typing (Arnaudov, 1978; Arnaudov et al., 2003; Arnaudov & Arnaudov, 2005). In Serbia, genotyping of *T. gondii* strains isolated from animals (sheep, pigs, pigeons) is in progress, and the first results confirm the dominance of type II strains

Earlier serological investigations of various animal species in SEE countries showed a prevalence of 37% for cattle, 30% for sheep, 26% for pigs, 17% for horses, 41% for dogs, 25% for cats, 52% for house mice and 20% for rats in Serbia, but except for pigs, they were carried out on samples of limited size (Šibalić, 1977). In Bulgaria, Nankov (1968) has shown a 15.7% prevalence in hares, and Arnaudov (1971, 1973) reported a prevalence of 32.6% for sheep

An overview of studies of *T. gondii* infection in animals in SEE countries in the last 20 years is presented in Table 2. Evidently, data are not available for a half of the SEE countries.

As in humans, and similar to the rest of Europe and elsewhere (Tenter et al., 2000; Hall et al., 2001), data on the prevalence in animals vary quite widely in SEE. The highest prevalence has been reported for cattle, sheep and goats (Table 2). While farming practices are similar throughout the SEE region, differences within the region mostly occur in the climatic

The single nation-wide survey on *T. gondii* infection in meat animals in SEE, performed recently in Serbia, showed high seroprevalence rates of 76.3% in cattle and 84.5% in sheep and a lower one, of 28.9%, in pigs (Klun et al., 2006). This study showed that cattle from Western Serbia were at an increased risk of infection compared to all other regions (Table 3), possibly associated with a comparably increased humidity in this region (Klun et al., 2006). The levels of specific antibody determined in the cattle were relatively low (not above 1:400),

**examined % Positive Test (cut-off) Origin of** 

Sheep unknown 0.5 DAT Nomadic al., 1994

Σ Goats 179 8.4 MAT (1:20) Σ

Σ Sheep 334 4.8 DAT Σ

Chickens 716 0.4 Bioassay Abattoir

Rats 142 1.4 Bioassay Pig farms

Sheep unknown 11.6 (sheep)

Goats 79 13.9 MAT (1:20) Farms Rajković-Janje et al., 1993 Goats 100 4 MAT (1:20) Farms

9.4 (lambs) DAT Farms

Sheep unknown 48.4 ELISA 10 farms Marinculić et al.,

Kutičić et al., 2005 Mice 86 0 Bioassay Pig farms +

**animals Ref.** 

Rajković-Janje et

1997

2000

households

Kutičić & Wikerhauser,

(unpublished data).

and 27.2% for goats.

conditions and terrain characteristics.

**Country Species No.** 

Croatia

The decreasing prevalence of *T. gondii* infection and a possible subsequent increase in the incidence of primary infections in pregnancy warrants introduction of CT prevention programs in the SEE countries. A prerequisite for such programs to be cost-effective, however, is an accurate assessment of the proportion of women of childbearing age susceptible to infection in pregnancy and the subsequent incidence of CT. These data are not yet available for most of the SEE, and are further complicated by the changing pattern of infection across the region. Thus, a sound and financially sustainable alternative that may be recommended for all of the SEE, similar to what has been recommended for Serbia (Bobić et al., 2003), includes health education of all women of childbearing age focusing on the locally significant risk factors for infection transmission in particular countries.

Health education is an adequate preventive measure for uninfected immunocompromised patients too.
