Risk factors that most strongly predicted acute infection in pregnant women were eating raw or undercooked lamb, beef, or “other” meat, contact with soil and travel outside Europe or the United States and Canada. Weaker associations, not significant at the 5% level, were observed for tasting raw meat during preparation of meals, eating salami, drinking unpasteurised milk, and working with animals. Contact with cats, kittens, cats' faeces, or cats who hunt for food was not a risk factor for infection.
The association between eating raw or undercooked meat and acute toxoplasma infection has been a consistent finding in previous studies. The types of meat, however, have varied. In a Norwegian study, undercooked lamb and pork but not beef were identified as risk factors,22
whereas in northern France beef or lamb but not pork were risk factors.26
Consumption of cured pork products was investigated in two studies, and both found a strong association with infection.21,26
Evidence from studies that used bioassays suggests that lamb, goat, pork, and game are more commonly infected than beef and that chicken rarely contains viable cysts.27–30
The risk of infected meat also depends on the age of the animal, the proportion of time the animal spent indoors,27
and the specific tissues used: non-skeletal muscle (heart, diaphragm, and tongue) has a higher density of cysts than skeletal muscle.32,33
Findings from biological studies can help to explain our results. Firstly, most pork is produced from pigs reared indoors and some would have been frozen. As freezing kills cysts the risk associated with eating raw or undercooked pork would be attenuated. Secondly, the pig meat used in salami is more likely to be infected because it includes non-skeletal muscle and may be derived from older animals farmed outdoors. The first report of the isolation of viable T gondii
from one of 67 samples of ready-to-eat cured meat in the United Kingdom34
showed that curing methods may not kill all tissue cysts35
or may not be stringently applied.
Thirdly, although T gondii
is rarely isolated from beef,32
the large amount consumed may explain the strong association with infection. Conversely, the association with tasting meat while cooking, which implies consumption of small quantities, may be due to tasting minced meat, which includes beef, lamb, or pork meat. The association between infection and unpasteurised milk or milk products was unexpected. T gondii
tachyzoites have been isolated from goats' milk and cows' colostrum28
but are destroyed within minutes by gastric juices.7
The association might be due to oocyst contamination by dirty production techniques or to confounding by other lifestyle factors (for example, eating undercooked organically produced meat).
Contact with soil or vegetables or fruit contaminated with soil was identified as a risk factor for toxoplasma infection in pregnancy in two of three studies that adjusted for confounders.21,22,26
Cats excrete oocysts (up to 10 million oocysts per day7
) for only two weeks of their life, when they first acquire infection. Oocysts become infective one to five days after excretion, are spread by surface water, and can survive for more than a year.28
Thus contact with soil and water, rather than direct contact with cats, is a risk factor for infection. The lack of an association with cat contact was also reported by two previous studies.22
Contact with cats was often mentioned as a risk factor whereas soil contact was rarely mentioned. Although we cannot exclude the possibility of recall bias, the negative and positive associations with cat and soil contact suggest that recall bias did not have a major effect. In addition, poor recall of exposures or varying interpretation of our questions may have attenuated the observed associations.
Population attributable fraction
Estimation of the population attributable fraction assumes that exposures have a net causal effect.20
We specified, a priori, a P value of
0.25 for inclusion of exposures “causally” associated with infection after adjustment for all relevant exposures. If the P value is set higher the population attributable fraction may be overexplained by irrelevant factors. If set too low some causal exposures may be excluded. Given our criteria, we failed to explain between 14% to 49% of infections in the different centres. The risk of infection after exposure to a risk factor did not vary significantly with centre, but the proportion of cases that could be attributed to each exposure did vary.
Public health action
The single most important health message for pregnant women in all centres in the study is to avoid eating any meat that has not been thoroughly cooked. The importance of other risk factors varied between centres. Consequently, advice to ensure that all fruit and vegetables are thoroughly washed and to avoid soil contact, working with animals, or drinking unpasteurised milk may be warranted but the advantages of comprehensive information must be balanced against the diminished emphasis on meat. Our results may not be generalisable to countries with different climates, farming, or culinary practices, particularly outside Europe, for which we recommend that local case-control studies are carried out to identify the main risk factors.
Although health information should be regarded as a right,36
many obstetric units have no policy on advice or information about toxoplasmosis.37–39
Where it is offered, information is often inconsistent,9,37
and ignorance, even among women in centres operating prenatal screening, is widespread.40
In a French study, only half of the susceptible women knew of more than one risk factor for toxoplasma infection, and 11% could not cite any.41
In our study, the proportion of women who could not cite any risk factors ranged from 2% in Brussels to 51% in Naples. A further concern is that knowledge may not lead to avoidance of exposure. In our study, lower rates of exposure were observed among women who mentioned raw meat as a risk factor but not among those who mentioned soil. Health promotion strategies must be based on an understanding of factors affecting women's behaviour.42
Information given by clinicians,26,43
or via the media45
may be more effective than written material.
Avoidance of infected meat could reduce the risk of infection during pregnancy by between 30% and 63%. To achieve this, health protection should be considered together with health promotion. Potential strategies include improved labelling of the source of meat and the type of processing (for example, farmed indoors or frozen) and measures to reduce infection in domestic animals (for example, improved farm hygiene).27
Although our study focused on pregnant women, postnatally acquired toxoplasmosis is an important cause of eye disease46
and can be fatal in immunocompromised patients.47
Health information and health protection strategies may be as relevant to the general public as they are to pregnant women.
What is already known on this topic
Eating undercooked meat or cured meat is a risk factor for toxoplasma infection
Contact with cats is not a risk factor for infection as excretion of oocysts is limited to only a few weeks
What this study adds
In six European centres eating undercooked, raw, or cured meat contributed to between 30% and 63% of infections, with soil contact contributing to up to 17% of infections
Action to reduce infection rates should include improved information about the risk associated with undercooked or cured meat, labelling of meat according to farming and processing methods, and measures to reduce infection in domestic animals