2009_infection With Toxoplasma Pregnancy

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R E V I E W A R T I C L E

Infection with Toxoplasma gondii during Pregnancy:Seroepidemiological Studies in AustriaR. Edelhofer1 and H. Prossinger2

1 Department of Pathobiology, Institute of Parasitology and Zoology, University of Veterinary Medicine, Vienna, Austria2 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 defining 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.

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

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: [email protected]

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 under-

taken 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 confinement 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 farmswhere 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 mut-

ton 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 modified agglutination test, were found in

36% of chickens from 12 Austrian biofarms. Because Austrians rarely con-

sume 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 differentpathways needs re-evaluation and targeted educational efforts to control

transmission.

Zoonoses and Public Health

18 2009 Blackwell Verlag GmbH Zoonoses Public Health. 57 (2010) 1826


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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 danger-

ous complication for HIV-positive individuals. Therefore,the assessment of its biological significance 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 preva-

lence 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 suf-

fered from prenatal Toxoplasma infection (Thalhammer,

1966, 1967, 1980). Thalhammer speculated that successful

intervention could become possible by screening of pre-

natal women, even if the infection prevalence could notbe lowered. Consequently, serological screening was intro-

duced 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 anti-

bodies in the first 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 pro-

portion 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 impor-

tance epidemiologically, and sources of infection vary

greatly among ethnicities. Knowledge of the most likely

sources of infection in a given population is a prerequisite

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 byingesting 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

fluorescence 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 gener-

ally 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


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In Austria, pork normally is not consumed raw or

undercooked, but there still remains an infection risk (pre-

dominantly for housewives among them expectant moth-

ers) 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 testingof 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 (Edelho-

fer et al., unpublished data). A significant 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 significant difference could be found between

antibody titres in the two age groups, whereas in sheep

antibody titres of 1 : 160 (17%) were found significantly

more often (P < 0.001) than 1 : 80 (13%) and antibody

titres of 1 : 320 (15.7%) were found significantly 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 aninfection prevalence of 61% in Bohemia.

Grazing animals (notably sheep and goats) face consid-

erable infection risk due to contamination of their envi-

ronment 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 1. Serological results of indirect fluorescent antibody testing for Toxoplasma gondii in pigs from five Austrian provinces slaughtered in

1982 and 1992

Province

1982 1992

n

n positive with end titres ofPositive n

(% positive) n

n positive with end titres ofPositive n

(% positive)1 : 16 1 : 64 1 : 256 1 : 1000 1 : 16 1 : 64 1 : 256 1 : 1000

Fattening pigs

Burgenland 94 9 4 2 1 16 (17.0) 264 2 1 0 0 3 (1.1)

Carinthia 197 1 1 0 0 2 (1.0)

Lower Austria 1022 61 3 1 1 66 (6.5) 1626 11 2 0 0 13 (0.8)

Upper Austria 908 97 26 19 5 147 (16.2) 170 0 0 0 0 0

Vienna 214 30 8 5 2 45 (21.0) 41 0 0 0 0 0

Totals 2238 197 41 27 9 274 (12.2) 2300 4 4 0 0 18 (0.8)

Breeding sows

Burgenland 113 21 18 7 3 49 (43.4) 18 1 0 0 0 1 (5.5)

Lower Austria 28 1 0 0 0 1 (3.6)

Total 113 21 18 7 3 49 (43.4) 46 2 0 0 0 2 (4.3)

Table 2. Seroprevalence of antibodies against Toxoplasma gondii by indirect fluorescent antibody test in sheep and goats in Austria tested in

19951996 by age category

Age group n n positive (%)

Positive for antibody titre (%)

1 : 40 1 : 80 1 : 160 1 : 320 1 : 640 1 : 1280 1 : 2500 1 : 5000 1 : 10 000

Sheep

2 years 2204 1737 (87.6) 12.3 16.3 21.9 20.0 7.4 12.5 7.0 2.5 12.7

Goats

2 years 254 191 (75.2) 1.9 20.5 25.0 28.1 6.5 4.5 4.5 2.5 4.0

Infection with Toxoplasma gondii during Pregnancy in Austria R. Edelhofer and H. Prossinger



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(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. gon-

dii in meat; however, raw goat and sheep milk are possi-

ble sources of human infection. We conclude thatmutton, rather than pork, must now be considered the

major source of meatborne Toxoplasma infections in

humans; especially because the seroprevalences in Aus-

trian pigs are low at least in conventionally (i.e. inten-

sive 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 impor-

tantly, viscera and meat scraps left at the site of dismem-

berment 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 num-

bers 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 seropreva-

lence in deer as evaluated by the indirect haemagglutina-

tion 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 esti-

mated 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 ani-

mals. 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 (Edel-

hofer et al., 1989, 1996). These findings indicate that

hunters need to be aware of possible T. gondii infections

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 antibodiesagainst 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%) pheas-

ants 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

briefly 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 inchickens 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 slaughter-

house 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 modified 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).

R. Edelhofer and H. Prossinger Infection with Toxoplasma gondii during Pregnancy in Austria

2009 Blackwell Verlag GmbH Zoonoses Public Health. 57 (2010) 1826 21


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In Austria, broilers destined for direct human con-

sumption do not exceed 1.5 kg body mass and are usually

7 weeks old, so infection with T. gondii is almost non-

existent. 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 infec-

tion when consuming conventionally raised chicken meat

is therefore very low.

The Importance and Prevalence of Toxoplasma

gondii in the Definitive 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 first outside

the body of the host, a process which usually takes 15 days,

dependent on temperature, moisture and other environ-

mental 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-specific anti-

bodies to determine their immune status (Lappin, 1996).

The ingestion of live bradyzoites is necessary to acquire

immunity to oocyst shedding because parentally adminis-

tered 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 oflatency (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 sero-

logical 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 significantly lower seroprevalences (P < 0.001)

than cats aged 12 years. Seventy-five per cent of cats

Table 3. Seroprevalence of Toxoplasma gondii antibodies as evaluated by the modified agglutination test in chickens from 12 farms in Austria

with free-ranging chickens

Farms n total on farm n tested n positive (%)

Antibody titres

1 : 10 1 : 20 1 : 40 1 : 80 1 : 160 1 : 320 1 : 640

A 1411 47 10 (21.2) 2 2 2 2 2

B 540 35 0 (0) 0 0 0 0 0C 1141 52 2 (3.8) 0 0 1 0 1

D 448 56 0 (0) 0 0 0 0 0

A + B 1411 + 540 86 5 (5.8) 1 0 1 0 3

E 434 37 0 (0) 0 0 0 0 0 0 0

F 874 58 1 (1.7) 1 0 0 0 0 0 0

G 392 47 40 (85.1) 20 11 6 1 1 1 0

H 732 131 125 (95.4) 9 15 30 26 16 13 16

I 3142 123 5 (4.0) 5 0 0 0 0 0 0

J 430 57 22 (38.5) 5 6 2 2 1 6

K 1000 50 42 (84.0) 2 21 2 2 3 12

L 500 51 50 (98.0) 5 14 9 7 3 12

Total 830 302 (36.3) 50 69 53 40 30 54 0

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




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older than 2 years were seropositive, significantly 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 significantly

with the cats age (r = 0.830) but was similar in Vienna

(67%) and other parts of Austria (70%), and did not dif-

fer by sex (Jiresch, 1998). Domestic cats that have no

chance to prey on rodents or birds have antibodies signif-

icantly (P < 0.001) less frequently (62%) than free-roam-

ing 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 signifi-

cantly (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 andBeattie (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 first

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 inocu-

lation 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 war-

rants considerable attention in future epidemiological

studies and ultimately in public education about interven-

tion 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, test-

ing 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.




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modelling seroprevalence decrease must have the same ana-

lytical 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 improve-

ment/sophistication of the model: while seropositivities in

pigs and cats were decreasing, the increasing numbers ofconsumed goats and sheep in Austria may halt the down-

ward 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 (first,

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

confirmation or rejection, based on the modelling of rates

along various/different epidemiological pathways (for fur-

ther details, see Tenter et al., 2000). The conventionally

suggested pathways seem tenuous and thus not contribut-

ing 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 dis-

tinct from modelling) involves the many possible contami-

nation pathways via sheep and goats. For example, more

Austrians (including pregnant women) now consume nat-

ural foods (i.e. organically grown plant foods and meat

from organically raised animals). Infection via knownpathways 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). Fur-

thermore, these individuals are predominantly members of

the lower socioeconomic classes, where high hygienic stan-

dards (especially in butcheries and slaughtering environs)

are difficult to maintain. In Austria, hygiene standards are

considered to be very high, irrespective of socioeconomic

status. The need to explain why infection numbers in preg-

nant women have not decreased as sharply as was expected

from the pig data (Table 1) is becoming more urgent

from both a scientific and a demographic point of view.

In the traditional Austrian lifestyle, beef consumption

was once considered a sign of affluence 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, corre-

late with the observed decrease in seropositivity propor-

tions in pregnant women. One often presented plausibility

argument (that affluent women experience fewer pregnan-

cies) fails on two counts: First, the demographic structure

of pregnant women is not routinely collected, collatedor recorded by the official Austrian statistics institutions

(cf. Statistik Austria). Second, affluent Austrians (irrespec-

tive of their cultural affinity) tend to consume foodstuffs

that do not exclude infection pathways very well (e.g. buy-

ing 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 col-

lected 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 thatsupport (traditional) plausibility arguments, much

remains to be done, because plausibility is insufficiently

rigorous to be useful for epidemiologically founded inter-

ventions. For example, field studies should not only mon-

itor 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 influence their food consumption life-

styles and to what extent their economic status correlates

with prevalence.

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