Anda di halaman 1dari 9

Zoonoses and Public Health


Infection with Toxoplasma gondii during Pregnancy: Seroepidemiological Studies in Austria

R. Edelhofer1 and H. Prossinger2
1 2

Department of Pathobiology, Institute of Parasitology and Zoology, University of Veterinary Medicine, Vienna, Austria Department of Anthropology, University of Vienna, Vienna, Austria

Impacts Seroepidemiological studies in livestock, chickens and wild game, and knowledge of consumption patterns of meats can aid in dening likely sources of meatborne pathways of Toxoplasma gondii infection in humans. Sheep and goat meat is becoming increasingly important as a potential source of Toxoplasma gondii infection in pregnant women in Austria, especially among Islamic communities. Most adult cats in Austria are T. gondii antibody positive, and cats remain an important potential source of infection.
Keywords: Toxoplasma gondii; seroepidemiology; domestic animals; wild mammals; pregnant women; cats; Austria Correspondence: R. Edelhofer. Department of Pathobiology, Institute of Parasitology and Zoology, University of Veterinary Medicine, Veterinarplatz 1, A-1210 Vienna, Austria. Tel.: +43 1 25077 2219; Fax: +43 1 25077 2290; E-mail: Received for publication August 15, 2008 doi: 10.1111/j.1863-2378.2009.01279.x

Summary Seropositivity among pregnant woman in Austria has decreased from 48% to 50% at the end of the 1970s to 35% in recent years. Despite this decrease, knowledge of possible sources and risk factors for Toxoplasma infection remains important. We reviewed seroepidemiological studies that were undertaken to assess the roles of undercooked meat and oocysts in cat faeces as potential sources of infection in pregnant women. Improved management and hygiene in pig herds raised in connement have resulted in less contact of pigs with cats and a decrease of infected pigs within one decade from 14% in 1982 to 0.9% in 1992. In Austrian wild boar populations, however, seroprevalences remained essentially unchanged during the same decade (18% in 1983 and 19% in 19901993). Austrian sheep and goats are usually kept on small farms where cats abound and are predominantly seropositive (66% in sheep and 69% in goats). The seroprevalence in cats has decreased from approximately 81% in 1987 to 59% in 1996; presumably because of cats increased consumption of processed food. Despite the decrease of infection in pregnant women via the cat-to-pig pathway, it may be offset by a recent concomitant increase in mutton consumption. Free-ranging chickens are a good indicator of the prevalence of T. gondii oocysts in the soil because chickens are ground feeders. Antibodies to T. gondii, as evaluated by the modied agglutination test, were found in 36% of chickens from 12 Austrian biofarms. Because Austrians rarely consume raw pork, the fraction of human T. gondii infections associated with pig meat consumption is likely small. As meat consumption and lifestyle patterns change in Austria, the risk of human infection with T. gondii via different pathways needs re-evaluation and targeted educational efforts to control transmission.

Introduction Toxoplasma gondii, a polyxenous protozoan parasite, has a facultatively heteroxenous life cycle and can probably

infect all warm-blooded animals (mammals and birds), including humans (Dubey and Beattie, 1988). Toxoplasma gondii is prevalent worldwide and is of veterinary and medical importance because it may cause abortion or

2009 Blackwell Verlag GmbH Zoonoses Public Health. 57 (2010) 1826

R. Edelhofer and H. Prossinger

Infection with Toxoplasma gondii during Pregnancy in Austria

congenital disease in its intermediate hosts (mammals). Because of its great importance as a zoonotic agent, T. gondii has been the most intensively studied coccidian parasite. Toxoplasmosis has received worldwide (medical) attention not only because it is a threat to pregnant women and their foetuses, but also because it is a dangerous complication for HIV-positive individuals. Therefore, the assessment of its biological signicance as a source of infection in warm-blooded animals remains important. There are still many details of the natural life cycle and the epidemiology of T. gondii infections about which little is known. Seroepidemiological studies assessing the prevalence of infection in intermediate hosts and of oocysts in cat faeces can provide useful insight into the potential role of these hosts in transmission. Prevalence of Toxoplasma gondii in Humans Toxoplasma gondii is estimated to infect up to one-third of the world population (Tenter et al., 2000). However, seroprevalence in human populations varies greatly among countries, geographical areas within one country and even ethnic groups living in the same geographical area. Studies during the last three decades have found a wide range of T. gondii antibody occurrence in human populations: from 0% to 100% (Dubey and Beattie, 1988; Tenter et al., 2000). In the 1950s and 1960s, 56% of Austrian babies suffered from prenatal Toxoplasma infection (Thalhammer, 1966, 1967, 1980). Thalhammer speculated that successful intervention could become possible by screening of prenatal women, even if the infection prevalence could not be lowered. Consequently, serological screening was introduced in 1975 as an obligatory test in Austrias prenatal screening programme (Flamm et al., 1975; Thalhammer, 1975). Every pregnant woman is tested for T. gondii antibodies in the rst trimester and, in case of seronegativity, again in the second and/or third trimester. With the introduction of this screening programme, the incidence of prenatal Toxoplasma infections decreased to 1 per 10 000 births (Aspock and Pollak, 1992). Seropositivity among pregnant women has decreased from 48% to 50% at the end of the 1970s, to 35% in recent years (1989 1991) (Aspock and Pollak, 1992). Unfortunately, the proportion of suspected primary infections during pregnancy has increased from less than 0.4% to a current estimate of 0.83% (Aspock et al., 1981, 1986, 2004; Aspock and Flamm, 1990; Aspock and Pollak, 1992; Edelhofer and Aspock, 1996; Edelhofer, 2004). Not all possible routes of infection are of equal importance epidemiologically, and sources of infection vary greatly among ethnicities. Knowledge of the most likely sources of infection in a given population is a prerequisite
2009 Blackwell Verlag GmbH Zoonoses Public Health. 57 (2010) 1826

for the development of effective strategies to decrease, and perhaps eliminate, infection risks. The Important Infection Pathways of Toxoplasma gondii in Livestock and Game Humans become infected post-natally with T. gondii by ingesting tissue cysts in uncooked or undercooked meat. The number of tissue cysts that may develop inside a host varies with the host species (Dubey et al., 1998; Dubey, 2000). Toxoplasma gondii has been found (predominantly encysted) in pig, sheep and goat tissues while viable cysts are rare in cattle (Dubey and Beattie, 1988). Prevalence of Toxoplasma gondii infections in pork In Europe, pork has been historically considered a major source of T. gondii infection in humans (Dubey, 1994) and tissue cysts have often been found in commercially available cuts of pork (Dubey et al., 1984, 1986; Dubey, 1986). In 1982 and 1992, blood samples were collected from 2351 and 2346 pigs, respectively (Edelhofer, 1994), and tested for serum antibodies to T. gondii using an indirect uorescence antibody (IFAT); 14% of pigs slaughtered in 1982 and 0.9% slaughtered in 1992 were seropositive for T. gondii (Edelhofer, 1994). Prevalence decreases have occurred in both fattening pigs and breeding sows (Table 1). Infection frequencies of fattening pigs are typically lower than those of breeding sows (Zimmermann et al., 1990; Dubey et al., 1991; Possardt, 1992). Pigs from large, modern fattening farms are typically slaughtered by 6 months, whereas pigs from small breeding farms generally live for several years. Thus, the risk of sows becoming infected is higher. In the Netherlands, van Knapen et al. (1982) found a prevalence of 11% in breeding sows, while fattening pigs tested negative. Likewise, in German pig farms with intensive management, the prevalence of T. gondii infection in pigs has decreased to <1% during the last decade (Tenter et al., 2000). These data imply that one can reduce the risk of T. gondii infection in pigs by using intensive farm management, with exclusion of cats and rodents from feed sources and from buildings housing pigs. Implementing such measures enables the production of pigs free of T. gondii, although this has been achieved in only a few countries, e.g. Austria (Edelhofer, 1994), the Netherlands (van Knapen et al., 1982) and Germany (Neurohr, 1982; Seineke, 1996). van Knapen et al. (1995) point out that the increase in prevalences from 1982 to 1995 in the Netherlands can be ascribed to management and housing deciencies.

Infection with Toxoplasma gondii during Pregnancy in Austria

R. Edelhofer and H. Prossinger

Table 1. Serological results of indirect uorescent antibody testing for Toxoplasma gondii in pigs from ve Austrian provinces slaughtered in 1982 and 1992 1982 n positive with end titres of Province Fattening pigs Burgenland Carinthia Lower Austria Upper Austria Vienna Totals Breeding sows Burgenland Lower Austria Total n 1 : 16 1 : 64 1 : 256 1 : 1000 Positive n (% positive) 1992 n positive with end titres of n 1 : 16 1 : 64 1 : 256 1 : 1000 Positive n (% positive)

94 1022 908 214 2238 113 113

9 61 97 30 197 21 21

4 3 26 8 41 18 18

2 1 19 5 27 7 7

1 1 5 2 9 3 3

16 (17.0) 66 147 45 274 (6.5) (16.2) (21.0) (12.2)

264 197 1626 170 41 2300 18 28 46

2 1 11 0 0 4 1 1 2

1 1 2 0 0 4 0 0 0

0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0

3 2 13 0 0 18

(1.1) (1.0) (0.8)


49 (43.4) 49 (43.4)

1 (5.5) 1 (3.6) 2 (4.3)

In Austria, pork normally is not consumed raw or undercooked, but there still remains an infection risk (predominantly for housewives among them expectant mothers) when tasting while preparing dishes in the kitchen. Prevalence of Toxoplasma gondii infections in mutton and goat meat Toxoplasma gondii causes abortion in small ruminants, with consequent economic losses for sheep and goat breeders (Dubey and Towle, 1986; Dubey and Beattie, 1988; Dubey, 1990). The seroprevalences of T. gondii in Austrian sheep and goats were estimated by IFAT testing of 4079 sheep and 687 goats. Antibodies against T. gondii were detected in 66% of sheep and 69% of goats, with positive titres ranging from 1 : 40 to 1 : 10 000 (Edelhofer et al., unpublished data). A signicant increase of T. gondii seroprevalence with age was evident for both sheep and goats (Table 2). The majority of sheep (n = 571) older than 2 years showed antibody titres of 1 : 160 and 1 : 320 (P < 0.001).

In goats, no signicant difference could be found between antibody titres in the two age groups, whereas in sheep antibody titres of 1 : 160 (17%) were found signicantly more often (P < 0.001) than 1 : 80 (13%) and antibody titres of 1 : 320 (15.7%) were found signicantly more often (P < 0.05) than 1 : 80 (13%). Seroprevalences for T. gondii in sheep are high, although they vary among regions and sampling periods (Tenter et al., 2000). Comparably high infection frequencies 74% tested by the Sabin-Feldman dye test (SFT) were found in the Czech Republic (Hejlcek and Literak, 1994) and in Poland (62% tested by SFT) (Ramisz and Zemburowa, 1978). For goats, Hejlcek and Literak (1994) found an infection prevalence of 61% in Bohemia. Grazing animals (notably sheep and goats) face considerable infection risk due to contamination of their environment with oocysts. The infection rates of these small ruminants are indicators for foodborne transmission risks, as tissue cysts have been found in many sheep tissues (Dubey and Kirkbridge, 1989; Lunden and Uggla, 1992). In the last two decades in Austria, the number of sheep

Table 2. Seroprevalence of antibodies against Toxoplasma gondii by indirect uorescent antibody test in sheep and goats in Austria tested in 19951996 by age category Positive for antibody titre (%) Age group Sheep <2 years >2 years Goats <2 years >2 years n n positive (%) 1 : 40 1 : 80 1 : 160 1 : 320 1 : 640 1 : 1280 1 : 2500 1 : 5000 1 : 10 000

598 2204 140 254

304 (50.8) 1737 (87.6) 60 (52.9) 191 (75.2)

14.2 12.3 4.0 1.9

13.6 16.3 19.8 20.5

18.7 21.9 21.2 25.0

17.1 20.0 26.5 28.1

9.3 7.4 4.0 6.5

14.8 12.5 2.5 4.5

8.5 7.0 1.3 4.5

3.3 2.5 2.6 2.5

0.6 12.7 17.2 4.0


2009 Blackwell Verlag GmbH Zoonoses Public Health. 57 (2010) 1826

R. Edelhofer and H. Prossinger

Infection with Toxoplasma gondii during Pregnancy in Austria

(goats) slaughtered for human consumption has increased from 215 000 (32 000) in 1983 to 351 000 (60 000) in 2007. During the same period, the numbers of pigs and cattle slaughtered decreased by about 15% and 24%, respectively. Cooking destroys infectious stages of T. gondii in meat; however, raw goat and sheep milk are possible sources of human infection. We conclude that mutton, rather than pork, must now be considered the major source of meatborne Toxoplasma infections in humans; especially because the seroprevalences in Austrian pigs are low at least in conventionally (i.e. intensive management) raised animals (Edelhofer, 1994). Prevalence of Toxoplasma gondii infections in game meat Tissue cysts of T. gondii in venison and other game meat, such as wild boar, hare, pheasant, etc., are a potential source of human infection (Dubey and Beattie, 1988), especially for hunters and their families. Transmission may occur when little care is taken while eviscerating and handling the game (Dubey, 1994) or when meat from these animals is served raw or undercooked. More importantly, viscera and meat scraps left at the site of dismemberment can be ingested by scavenging cats which then shed oocysts in their faeces, thereby contaminating the environment with T. gondii. Deer are the most commonly bagged game species in Austria. For example, in the 2006/2007 season, the numbers of roe deer (Capreolus capreolus), European hare (Lepus europaeus), pheasants (Phasianus colchicus) and wild boar (Sus scrofa) reported as being harvested (data obtained from Statistik Austria, Vienna) were 258 264, 125 400, 123 604 and 18 540, respectively. The seroprevalence in deer as evaluated by the indirect haemagglutination assay (IHA) was reported to be 12% (Edelhofer, 2004). This seroprevalence is similar to that reported in the Czech Republic by Hejlcek et al. (1997). Kapperud (1978) and Vikoren et al. (2004) pointed out that roe deer remains a source of infection for humans in Norway and Sweden. Wild boar (Sus scrofa) is a good indicator species for monitoring T. gondii environmental contamination. In the last three decades, the population of wild boar increased in almost all European countries and is estimated to be over one million individuals in the European Union (Laddomada, 2000). Antibodies to T. gondii in Europe have been reported in the Czech Republic (Hejlcek et al., 1997) in 15% (n = 124) of bagged animals. In Austria, wild boars were tested for antibodies against T. gondii. In 1983 and 19901993, 18% and 19% of wild boars were antibody positive, respectively (Edelhofer et al., 1989, 1996). These ndings indicate that hunters need to be aware of possible T. gondii infections
2009 Blackwell Verlag GmbH Zoonoses Public Health. 57 (2010) 1826

in game and ensure thorough cooking of meat prior to its consumption. Pheasants and hares should also be good indicators of soil contamination with T. gondii oocysts because they are ground feeders. There are few published estimates of the seroprevalence of T. gondii infection in pheasants, of 409 pheasants shot in Austria and tested for antibodies against T. gondii by IHA, only 4% were found to be sero positive (Edelhofer et al., 1989; Edelhofer, 2004). Literak et al. (1992) isolated T. gondii from 6 of 306 (2%) pheasants in the Czech Republic. A decline in numbers of European hares has been reported in several European countries since the 1960s. Various infectious diseases of hares have been implicated in this decline (Frolich et al., 2003). In Austria, sera of 3124 hares were tested by IHA, but only 2% (Edelhofer et al., 1989; Edelhofer, 2004) were found to be seroposi tive. In the Czech Republic, Hejlcek et al. (1997) tested 293 hares and found 5% to be seropositive. Only well-cooked meat of pheasants, hares and wild boar is consumed in Austria, so ingested T. gondii cysts in tissues of these game animals are most unlikely to be infective. One exception is an Austrian specialty called Rehnusschen, a dish of roe deer venison that is only briey roasted and slightly bloody. This would be a potential source of human infection with T. gondii in Austria. Prevalence of Toxoplasma gondii infections within chicken meat A worldwide study of T. gondii population structure in chickens based on isolation and genotyping was initiated in the last decade (Dubey et al., 2009, this volume). In Austria, samples of chickens were collected in a slaughterhouse that processed 4000 chickens (from so-called organic farms) per hour. Such free-range chickens live longer than 1 year before slaughter (Dubey et al., 2005). Heart blood and heart muscles were collected. The heart was chosen because it is highly indicative of T. gondii infection in chickens (Dubey et al., 2004). Antibodies to T. gondii assayed by modied agglutination test (MAT) were found in 36% of chickens (Table 3). In one farm, the seroprevalence was very high 95% (n = 131). On this farm, no cats had access to the chicken housing area but were known to defecate in chicken feed stored in open bins. By implication, raising chickens in wired cages with feed mixed at a central plant reduces the risk of T. gondii infection. The recent trend of raising free-range chickens increases the risk of T. gondii infection (Dubey et al., 2005), as T. gondii can be present in the eggs of free-range chickens, presenting a source of infections for humans (Jacobs and Melton, 1966).

Infection with Toxoplasma gondii during Pregnancy in Austria

R. Edelhofer and H. Prossinger

Table 3. Seroprevalence of Toxoplasma gondii antibodies as evaluated by the modied agglutination test in chickens from 12 farms in Austria with free-ranging chickens Antibody titres Farms A B C D A+B E F G H I J K L Total n total on farm 1411 540 1141 448 1411 + 540 434 874 392 732 3142 430 1000 500 n tested 47 35 52 56 86 37 58 47 131 123 57 50 51 830 n positive (%) 10 0 2 0 5 0 1 40 125 5 22 42 50 302 (21.2) (0) (3.8) (0) (5.8) (0) (1.7) (85.1) (95.4) (4.0) (38.5) (84.0) (98.0) (36.3) 1 : 10 2 0 0 0 1 0 1 20 9 5 5 2 5 50 1 : 20 2 0 0 0 0 0 0 11 15 0 6 21 14 69 1 : 40 2 0 1 0 1 0 0 6 30 0 2 2 9 53 1 : 80 2 0 0 0 0 0 0 1 26 0 2 2 7 40 1 : 160 2 0 1 0 3 0 0 1 16 0 1 3 3 30 1 : 320 1 : 640

0 0 1 13 0 6 12 12 54

0 0 0 16 0

A + B refers to a joint sample from farms A and B.

In Austria, broilers destined for direct human consumption do not exceed 1.5 kg body mass and are usually 7 weeks old, so infection with T. gondii is almost nonexistent. 1-year-old chicken carcasses are not sold directly to Austrian consumers but are mainly used for baby food and soups. The probability of acquiring Toxoplasma infection when consuming conventionally raised chicken meat is therefore very low. The Importance and Prevalence of Toxoplasma gondii in the Denitive Host: the Cat Fundamental to transmission of T. gondii is the cat. Cats shed unsporulated oocysts after ingesting any one of these infectious stages of T. gondii: tachyzoites in groups, bradyzoites in tissue cysts and sporozoites in oocysts. The pre-patent period (days to shedding oocysts) differs after ingestion of bradyzoites or oocysts (Dubey and Frenkel, 1976). Almost every cat sheds oocysts after ingesting tissue cysts, whereas less than half the cats shed oocysts after ingesting oocysts (Dubey and Frenkel, 1976). Oocysts are not immediately infectious and most sporulate rst outside the body of the host, a process which usually takes 15 days, dependent on temperature, moisture and other environmental conditions (Dubey et al., 1970). The high frequency of seropositivity in a cat population contrasts sharply with the low prevalences of oocysts in faeces; as low as 0.52% in Europe (Dubey and Beattie, 1988; Tenter et al., 2000). Serological testing of cats Cats can be tested serologically for T. gondii-specic antibodies to determine their immune status (Lappin, 1996).

The ingestion of live bradyzoites is necessary to acquire immunity to oocyst shedding because parentally administered T. gondii (of any stage) do not induce protective immunity to oocyst shedding in cats (Frenkel and Smith, 1982). A serologically positive result implies that the cat had already been infected with T. gondi (Tenter et al., 2000). Most cats with detectable levels of IgG antibodies to T. gondii are likely to be immune and thus will not excrete oocysts for quite some time (Tenter et al., 2000). Cats that have been infected via tissue cysts usually seroconvert (IgG) 25 weeks post-infection, i.e. after the period of latency (Dubey and Thulliez, 1989; Omata et al., 1990; Dubey et al., 1995). However, in some cats that have been infected by ingestion of oocysts, IgG antibodies are already detectable during the extended period of pre-latency (Dubey, 1996). While detection of IgG antibodies in the serum of cats is mostly indicative of immunity, it does not preclude the possibility of shedding of oocysts. In addition, some previously infected cats may re-shed oocysts for short periods of time (Tenter et al., 2000). In domestic cats, antibodies to T. gondii may be detected in up to 74% of adult cat populations, depending on how they are fed and whether they are kept indoors or outdoors (Tenter et al., 2000). Seroprevalences are usually higher in stray or feral cats than in domestic ones. However, 946% of pet cats in Europe, South America and USA have serological evidence of past exposure to the parasite (Dubey and Beattie, 1988; Tenter et al., 2000). In Austria, from 1995 to 1996, 53% of cats were sero positive (Edelhofer and Aspock, 1996). Cats younger than 1 year had signicantly lower seroprevalences (P < 0.001) than cats aged 12 years. Seventy-ve per cent of cats
2009 Blackwell Verlag GmbH Zoonoses Public Health. 57 (2010) 1826

R. Edelhofer and H. Prossinger

Infection with Toxoplasma gondii during Pregnancy in Austria

older than 2 years were seropositive, signicantly more than cats 12 years old (P < 0.002). To test whether there are trends in infection frequencies within the last decade, 2049 sera (about 200 cats each year in an age range of 4 weeks to 18 years with a comparable age distribution each year) were examined for antibodies against T. gondii using IFAT (Edelhofer and Aspock, 1996; Jiresch, 1998; Edelhofer, 2004). Seropositivity increased signicantly with the cats age (r = 0.830) but was similar in Vienna (67%) and other parts of Austria (70%), and did not differ by sex (Jiresch, 1998). Domestic cats that have no chance to prey on rodents or birds have antibodies significantly (P < 0.001) less frequently (62%) than free-roaming cats (76%). The age breakdown: 35% of cats younger than one year, 54% of those aged 12 years, 75% of cats aged 23 years and 100% of cats older than 3 years (n = 70) were seropositive (Jiresch, 1998). In Austria, the seroprevalence in cats decreased signicantly (P < 0.01) from 76% in 1986 to 59% in 1995. With increased feeding of canned and dry food, this decrease may continue. In 1990, 25 608 tons of canned food were sold in Austria (estimated cat population of 1.33 million) and sales increased to 73 183 tons in 2007 for an estimated cat population of 2.07 million (Fig. 1; proprietary data supplied by market research companies). Coproscopical examinations of cats Felidae are important dispersers of T. gondii because they are the only species that excretes T. gondii oocysts (Miller et al., 1972). Worldwide prevalence data on T. gondii oocysts in feline faeces are summarized in Dubey and Beattie (1988). More recent studies for cats in Europe has been published by Schares et al. (2008) and in the USA by Dubey and Jones (2008). The proportion of cats excreting oocysts at any time is usually not more than 1% in most countries (Dubey, 1995, 2004). However, a

cat may shed millions of oocysts during its lifetime, and these oocysts are very hardy, capable of surviving in the soil for over a year (Dubey and Beattie, 1988), so the risk of infection is obvious. Cats can be infected by ingesting oocysts, but experiments have shown that they are more commonly infected by ingestion of tissue cysts present in their prey (Dubey and Frenkel, 1976; Dubey, 2001, 2006). Obviously, T. gondii infection prevalences are greater in rural than in town cats and in stray than in domestic cats (Dubey and Beattie, 1988). After a primary infection with T. gondii, cats usually shed large numbers of oocysts (20150 million) for a brief period (Dubey and Frenkel, 1972). Conventional wisdom claims that shedding of oocysts after re-infection with T. gondii is rare (Dubey and Frenkel, 1972, 1974), but recent studies showed that this putative immunity is not lifelong (Dubey, 1995). A second shedding of oocysts could be induced in cats that were challenged with T. gondii about 6 years after the rst infection (Dubey, 1995; Dubey et al., 1995). Occasionally, short-term re-shedding of oocysts has been observed without re-infection of the cat (Lappin, 1994). In the course of our routine diagnoses at the Institute of Parasitology and Zoology, University of Veterinary Medicine in Vienna, 5872 cat faeces samples were tested coproscopically. Between 1990 and 2003, 1% of samples contained oocysts of the type Toxoplasma/Hammondia. It is not possible to distinguish microscopically between T. gondii and Hammondia hammondii and mouse inoculation was not used to distinguish the parasites. We note that the serological and faecal prevalence estimates for cats in Austria are comparable with the results of other European countries (Dubey and Beattie, 1988). In Austria, the high seroprevalence (53%) estimate contrasts sharply with the estimated 1% of cats excreting oocysts. However, these data indicate that every second cat is likely to shed Toxoplasma oocysts at least once during its lifetime and this with a magnitude of 107108 (Dubey and Frenkel, 1972). This source of infection warrants considerable attention in future epidemiological studies and ultimately in public education about intervention strategies. Discussion From the 1970s to the 1990s, seroprevalence in pigs decreased sharply from 14% to 0.9% and was accompanied by a less marked decrease in seropositivity of cats from 81% to 59%. These decreases likely contributed to the decrease in seropositivity in Austrian pregnant women (from 49% to 35%) during the same period. However, testing this putative explanation requires careful modelling. If the infection probability of pregnant women remains constant during these two decades, then the function

Fig. 1. The increase in the cat population in Austria between 1990 and 2005. The (cubic) regression only helps to visually accentuate the trend; no statistical inferences are made with this regression.

2009 Blackwell Verlag GmbH Zoonoses Public Health. 57 (2010) 1826

Infection with Toxoplasma gondii during Pregnancy in Austria

R. Edelhofer and H. Prossinger

modelling seroprevalence decrease must have the same analytical form in either case (pig and cat seropositivity). This analytical form is presently unknown, as data points within the two decades are too sparse. Even if more data points were known, a further complication requires improvement/sophistication of the model: while seropositivities in pigs and cats were decreasing, the increasing numbers of consumed goats and sheep in Austria may halt the downward trend of seroprevalence in pregnant women. Sagel and Kaindl (2006) found a decrease of 0.635% per year. This was extrapolated to a value of 12.7% over two decades, which is evidence that the decrease is not as marked as is to be expected from the decrease in seropositivity in cats and pigs. The conventional suite of plausibility arguments (rst, pregnant women are infected by ingesting vegetables contaminated with oocysts from garden soils and second, pregnant women are infected by ingesting tissue cysts while tasting incompletely cooked dishes in the kitchen) requires conrmation or rejection, based on the modelling of rates along various/different epidemiological pathways (for further details, see Tenter et al., 2000). The conventionally suggested pathways seem tenuous and thus not contributing to the observed high proportion of seropositivity still prevalent in pregnant women. A closer evaluation of the data and the modelling with various regression functions is needed. A further line of epidemiological investigations (as distinct from modelling) involves the many possible contamination pathways via sheep and goats. For example, more Austrians (including pregnant women) now consume natural foods (i.e. organically grown plant foods and meat from organically raised animals). Infection via known pathways must be monitored by an obligatory registration/ census system. Furthermore, demographic percentages of infection do not differentiate the statistical weightings of ethnicity-related pathways. An increasing segment of the Austrian population is either Islamic or maintains an Islam-derived lifestyle (4.23% in 2001 compared to 2.04% in 1991 and 1.02% in 1981) and their diet includes a high consumption of mutton and goat meat (and no pork). Furthermore, these individuals are predominantly members of the lower socioeconomic classes, where high hygienic standards (especially in butcheries and slaughtering environs) are difcult to maintain. In Austria, hygiene standards are considered to be very high, irrespective of socioeconomic status. The need to explain why infection numbers in pregnant women have not decreased as sharply as was expected from the pig data (Table 1) is becoming more urgent from both a scientic and a demographic point of view. In the traditional Austrian lifestyle, beef consumption was once considered a sign of afuence and therefore often associated with unusual events in life (e.g. festivities). Although no longer so, beef consumption remains an

exceptional event feature for Islamic immigrants in Austria. The rise of beef consumption does not, apparently, correlate with the observed decrease in seropositivity proportions in pregnant women. One often presented plausibility argument (that afuent women experience fewer pregnancies) fails on two counts: First, the demographic structure of pregnant women is not routinely collected, collated or recorded by the ofcial Austrian statistics institutions (cf. Statistik Austria). Second, afuent Austrians (irrespective of their cultural afnity) tend to consume foodstuffs that do not exclude infection pathways very well (e.g. buying directly from organic farms, more frequent incidences of eating on vacations/business trips abroad, as well as more numerous occurrences of feasting on game). Conclusion Seropositivity of foodstuffs derived from intermediate hosts remains a source of infection in pregnant women, with little signs of abating. Indeed, infection prevalences are currently increasing. Although the Austrian prenatal screening programme does attempt to medically intervene (and thus prevent infection of the foetus) when a pregnant woman is seropositive, a more effective strategy would be to control, and perhaps eliminate, transmission pathways. Elimination, however, necessitates (as a pre-requisite) detailed knowledge of the dominant infection pathways. As this review shows, much prevalence data have been collected and collated, but the (model) parameters that could lead to eradication strategies remain elusive. Plausibility arguments are of very limited usefulness here. While this review presents numerous trend data that support (traditional) plausibility arguments, much remains to be done, because plausibility is insufciently rigorous to be useful for epidemiologically founded interventions. For example, eld studies should not only monitor the prevalences in pregnant women, but also collect data as to what foodstuffs (including whether organically grown, and/or whether halal-raised and -slaughtered sheep and goats, etc.) they consume, to what extent their religious practices inuence their food consumption lifestyles and to what extent their economic status correlates with prevalence. References
Aspock, H., and H. Flamm, 1990: 15 Jahre Toxoplasmose Uberwachung der Schwangeren in Osterreich. Ein bei spielgebender Erfolg bei der Verhutung von Infektionen des Ungeborenen. Osterr. Apotheker Ztg. 44, 447448. Aspock, H., and A. Pollak, 1992: Prevention of prenatal toxoplasmosis by serological screening of pregnant women in Austria. Scand. J. Infect. Dis. 84(Suppl.), 3238.

2009 Blackwell Verlag GmbH Zoonoses Public Health. 57 (2010) 1826

R. Edelhofer and H. Prossinger

Infection with Toxoplasma gondii during Pregnancy in Austria

Aspock, H., O. Picher, H. Flamm, and H. Auer, 1981: Aktuelle Probleme der Serodiagnostik im Rahmen der Toxoplas mose-Uberwachung wahrend der Schwangerschaft. Mitt. Osterr. Ges. Parasitol. 3, 2025. Aspock, H., H. Flamm, and O. Picher, 1986: Die Toxoplas mose-Uberwachung wahrend der Schwangerschaft 10 Jah re Erfahrungen in Osterreich. Mitt. Osterr. Ges. Parasitol. 8, 105113. Aspock, H., H. Auer, and J. Walochnik, 2004: Die Pravention der pranatalen Toxoplasmose: Strategien, Stand der Kenntnis, aktuelle Probleme. Nova Acta Leopold. 89, 334. Dubey, J. P., 1986: A review of toxoplasmosis in pigs. Vet. Parasitol. 19, 181223. Dubey, J. P., 1990: Status of toxoplasmosis in sheep and goats in the United States. J. Am. Vet. Med. Assoc. 196, 259262. Dubey, J. P., 1994: Toxoplasmosis. J. Am. Vet. Med. Assoc. 2005, 15931598. Dubey, J. P., 1995: Duration of immunity to shedding of Toxoplasma gondii oocysts by cats. J. Parasitol. 81, 410 415. Dubey, J. P., 1996: Infectivity and pathogenicity of Toxoplasma gondii oocysts for cats. J. Parasitol. 82, 957961. Dubey, J. P., 2000: The scientic basis for prevention of Toxoplasma gondii infection: studies on tissue cyst survival, risk factors and hygiene measures. In: Ambroise-Thomas, P., and E. Petersen (eds), Congenital Toxoplasmosis: Scientic Background, Clinical Management and Control, pp. 271275. Springer-Verlag, Paris. Dubey, J. P., 2001: Oocyst shedding in cats fed isolated bradyzoites and comparison of infectivity of bradyzoites of the VEG strain Toxoplasma gondii in cats and mice. J. Parasitol. 87, 215219. Dubey, J. P., 2004: Toxoplasmosis a waterborne zoonosis. Vet. Parasitol. 126, 5772. Dubey, J. P., 2006: Comparative infectivity of oocysts and bradyzoites and comparison of infectivity of bradyzoites of Toxoplasma gondii for intermediate (mice) and denitive (cats) hosts. Vet. Parasitol. 140, 6975. Dubey, J. P., and C. P. Beattie, 1988: Toxoplasmosis of Animals and Man. CRC Press, Boca Raton, FL. Dubey, J. P., and J. K. Frenkel, 1972: Cyst-induced toxoplasmosis in cats. J. Protozool. 19, 155177. Dubey, J. P., and J. K. Frenkel, 1974: Immunity to feline toxoplasmosis: modication by administration of corticosteroids. Vet. Pathol. 11, 350379. Dubey, J. P., and J. K. Frenkel, 1976: Feline toxoplasmosis from actually infected mice and the development of Toxoplasma cysts. J. Protozool. 23, 537546. Dubey, J. P., and C. A. Kirkbridge, 1989: Economic and public health considerations of congenital toxoplasmosis in lambs. J. Am. Vet. Med. Assoc., 195, 17151716. Dubey, J. P., and P. Thulliez, 1989: Serological diagnosis of toxoplasmosis in cats fed Toxoplasma gondii tissue cysts. J. Am. Vet. Med. Assoc. 194, 12971299.

Dubey, J. P., and A. Towle, 1986: Toxoplasmosis in sheep a review and annotated bibliography. Misc. Publ. No. 10. Commonwealth Inst. of Parasitol., London. Am. J. Vet. Res. 47, 523524. Dubey, J. P., N. L. Miller, and J. K. Frenkel, 1970: The Toxoplamsma gondii oocysts from cat feces. J. Exp. Med. 132, 636662. Dubey, J. P., K. D. Murrell, and R. Fayer, 1984: Persistence of encysted Toxoplasma gondii in tissues of pigs fed oocysts. Am. J. Vet. Res. 45, 19411943. Dubey, J. P., K. D. Murrell, and R. Fayer, 1986: Distribution of Toxoplasma gondii tissue cysts in commercial cuts of pork. J. Am. Vet. Med. Assoc. 188, 10351037. Dubey, J. P., J. C. Leighty, V. C. Beal, W. R. Anderson, C. D. Andrews, and P. Thulliez, 1991: National seroprevalence of Toxoplasma gondii in pigs. J. Parasitol. 77, 517521. Dubey, J. P., M. R. Lappin, and P. Thulliez, 1995: Long-term antibody responses of cats fed Toxoplasma gondii tissue cysts. J. Parasitol. 81, 887893. Dubey, J. P., D. S. Lindsay, and C. A. Speer, 1998: Structures of Toxoplasma gondii tachyzoites, bradyzoites, and sporozoites and biology and development of tissue cysts. Clin. Microbiol. Rev. 11, 267299. Dubey, J. P., M. Levy, C. Sreekumar, O. C. H. Kwok, S. K. Shen, E. Dahl, P. Thulliez, and T. Lehmann, 2004: Tissue distribution and molecular characterization of chicken isolates of Toxoplasma gondii from Peru. J. Parasitol. 90, 10151018. Dubey, J. P., R. Edelhofer, P. Marcet, M. C. B. Vianna, O. C. H. Kwok, and T. Lehmann, 2005: Genetic and biologic characteristics of Toxoplasma gondii infections in free-range chickens from Austria. Vet. Parasitol. 133, 299306. Dubey, J. P., and J. L. Jones, 2008: Toxoplasma gondii infection in humans and animals in the United States. Int. J. Parasit. 38, 12571278. Edelhofer, R., 1994: Prevalence of antibodies against Toxoplasma gondii in pigs in Austria an evaluation of data from 1982 and 1992. Parasitol. Res. 80, 642644. Edelhofer, R., 2004: Seroepidemiologische Studien zur Toxo plasmose aus human- und veterinarmedizinischer Sicht eine Retrospektive der letzten 25 Jahre in Osterreich. In: Entomologie und Parasitologie, Vol. 3, Denisia OO Landesmuseum, Linz, pp. 411417. Edelhofer, R., and H. Aspock, 1996: Infektionsquellen und Infektionswege aus der Sicht des Toxoplasmose-Screenings der Schwangeren in Osterreich. Mitt. Osterr. Ges. Parasitol. 18, 5970. Edelhofer, R., E. M. Heppe, A. Hassl, and H. Aspock, 1989: Toxoplasma-Infektionen bei jagdbaren Wildtieren in Ostost erreich. Mitt. Osterr. Ges. Parasitol. 11, 119123. Edelhofer, R., H. Prosl, and E. Kutzer, 1996: Zur Trichinellose und Toxoplasmose der Wildschweine in Ostosterreich. Wr. Tierarztl. Mschr. 83, 225229. Flamm, H., H. Aspock, O. Picher, and H. Werner, 1975: Die Toxoplasmose-Untersuchung von Schwangeren und Neuge borenen. Osterr. Arzteztg. 30, 1517.

2009 Blackwell Verlag GmbH Zoonoses Public Health. 57 (2010) 1826


Infection with Toxoplasma gondii during Pregnancy in Austria

R. Edelhofer and H. Prossinger

Frenkel, J. K., and D. D. Smith, 1982: Immunization of cats against sheeding of Toxoplasma oocysts. J. Parasitol., 38, 744748. Frolich, K., J. Wisser, H. Schmuser, U. Fehlberg, H. Neubauer, R. Grunow, K. Nikolau, J. Priemer, S. Thiede, W. J. Streich, and S. Speck, 2003: Epizootiologic and ecologic investigations of european brown hares (Lepus europaeus) in selected populations from Schleswig-Holstein, Germany. J. Wildl. Dis. 39, 751761. Hejlcek, K., and I. Literak, 1994: Incidence and prevalence of toxoplasmosis among sheep and goats in southern and western Bohemia. Acta Vet. Brno. 63, 151159. Hejlcek, K., I. Literak, and J. Nezval, 1997: Toxoplasmosis in wild mammals from the Czech Republic. J. Wildl. Dis. 33, 480485. Jacobs, L., and M. L. Melton, 1966: Toxoplasmosis in chickens. J. Parasitol. 52, 11581162. Jiresch, W., 1998: Zur Toxoplasmose der Katzen in Osterreich: Ein Vergleich der Jahre 1986-1995. Thesis. Vet. Med. Univ. Wien, Vienna. Kapperud, G., 1978: Survey for toxoplasmosis in wild and domestic animals from Norway and Sweden. J. Wildl. Dis. 14, 157162. van Knapen, F., J. H. Franchimont, and G. van der Lugt, 1982: Prevalence of antibodies to Toxoplasma in farm animals in the Netherlands and its implication for meat inspection. Vet. Q. 4, 101105. van Knapen, F., A. F. T. Kremers, J. H. Franchimont, and U. Narucka, 1995: Prevalence of antibodies to Toxoplasma gondii in cattle and swine in the Netherlands: towards an integrated control of livestock production. Vet. Q. 17, 8791. Laddomada, A., 2000: Incidence and control of CSF in wild boar in Europe. Vet. Microbiol. 73, 121130. Lappin, M. R., 1994: Diagnosis and management of feline toxoplasmosis. Vet. Technician, 15, 109115. Lappin, M. R., 1996: Feline toxoplasmosis: interpretation of diagnostic test results. Semin. Vet. Med. Surg. (Small Anim.) 11, 154160. Literak, I., K. Hejlcek, J. Nezval, and c. Folk, 1992: Incidence of Toxoplasma gondii in populations of wild birds in Czech Republic. Avian Pathol. 21, 659665. Lunden, A., and A. Uggla, 1992: Infectivity of Toxoplasma gondii in mutton following cruing, smoking, freezing or microwave cooking. Int. J. Food Microbiol. 15, 357363. Miller, N. L., J. K. Frenkel, and J. P. Dubey, 1972: Oral infections with Toxoplasma cysts and oocysts in felines, other mammals, and in birds. J. Parasitol. 58, 928937.

Neurohr, B. 1982: Latente Toxoplasma-Infektionen bei Schwei nen in Suddeutschland sowie Moglichkeiten des Nachweisese mit dem Indirekten Fluoreszenztest und der Indirekten Hamagglutination. Thesis. Vet. Med Univ. Munchen, Munich. Omata, Y., H. Oikawa, M. Kanada, K. Mikazuki, T. Nakabayashi, and N. Suzuki, 1990: UExperimental feline toxoplasmosis: humural immune responses of cats inoculated orally with cysts and oocysts. Jpn. J. Vet. Sci. 62, 865867. Possardt, C., 1992: Untersuchungen zur Toxoplasma gondiiInfektion in einer Schweinegroanlage mit verschiedenen serodiagnostischen Verfahren. Thesis, Humboldt Univ., Berlin. Ramisz, A., and K. Zemburowa, 1978: Serological Survey of Toxoplasma Antibodies in Animal Livestock.. Short Communication. 4th Int. Congr. Parasitol., Warsaw, Section E, p. 85. Sagel, U., and M. Kaindl, 2006: Epidemiology of Toxoplasmo sis in Pregancy in Upper Austria 20002005. Mitt. d. Osterr. Ges. f. Tropenmed. u. Parasitol, Linz, p. 47. Schares, G., M. V. Vrhovec, N. Pantchev, D. C. Herrmann, and F. J. Conraths, 2008: Occurrence of Toxoplasma gondii in the faeces of cats from Germany and other European countries. Vet. Parasitol. 152, 3445. Seineke, P., 1996: Seropravalenz von Antikorpern gegen Toxoplasma gondii bei Schafen, Ziegen und Schweinen in Niedersachsen. Thesis. Vet. Med. Univ., Hannover. Tenter, A. M., A. R. Heckeroth, and L. M. Weiss, 2000: Toxoplasma gondii: from animals to humans. Int. J. Parasitol. 30, 12171258. Thalhammer, O., 1966: Die angeborene Toxoplasmose. In: Kirchhoff, H., and H. Kraubig (eds), Toxoplasmose, pp. 167177. Praktische Fragen und Ergebnisse, Stuttgart, G. Thieme. Thalhammer, O., 1967: Pranatale Erkrankungen des Menschen. Stuttgar, G. Thieme, p. 442. Thalhammer, O., 1975: Die Toxoplasmose-Untersuchung von Schwangeren und Neugeborenen. Wr. Klin. Wschr. 87, 676 681. Thalhammer, O., 1980: Toxoplasmose in der Schwangerschaft. Mitt. d. Osterr. Sanitatsverwaltung 81, 124127. Vikoren, T., J. Tharaldsen, B. Fredriksen, and K. Handeland, 2004: Prevalence of Toxoplasma gondii in wild red deer, roe deer, moose, and reindeer from Norway. Vet. Parasitol. 120, 159169. Zimmermann, J. J., D. W. Dreesen, W. J. Owen, and G. W. Beran, 1990: Prevalence of toxoplasmosis in swine from Iowa. J. Am. Vet. Med. Assoc. 196, 266270.


2009 Blackwell Verlag GmbH Zoonoses Public Health. 57 (2010) 1826