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Prenatal education for congenital toxoplasmosis

  1. Simona Di Mario1,*,
  2. Vittorio Basevi1,
  3. Carlo Gagliotti2,
  4. Daniela Spettoli1,
  5. Gianfranco Gori1,
  6. Roberto D'Amico3,
  7. Nicola Magrini4

Editorial Group: Cochrane Pregnancy and Childbirth Group

Published Online: 28 FEB 2013

Assessed as up-to-date: 15 MAY 2012

DOI: 10.1002/14651858.CD006171.pub3


How to Cite

Di Mario S, Basevi V, Gagliotti C, Spettoli D, Gori G, D'Amico R, Magrini N. Prenatal education for congenital toxoplasmosis. Cochrane Database of Systematic Reviews 2013, Issue 2. Art. No.: CD006171. DOI: 10.1002/14651858.CD006171.pub3.

Author Information

  1. 1

    Regional health authority of Emilia-Romagna, SaPeRiDoc, Primary health care, general medicine, planning and development of health services, Bologna, Italy

  2. 2

    Regional agency for health and social care of Emilia-Romagna, Control of infectious disease Unit, Bologna, Italy

  3. 3

    University of Modena and Reggio Emilia, Statistics Unit, Department of clinical and diagnostic medicine and public health, University of Modena and Reggio Emilia, Modena, Italy, Modena, Italy

  4. 4

    WHO Collaborating Centre for Evidence-based Research Synthesis and Guideline Development, Regional Agency for Health and Social Care of Emilia-Romagna, Drug Evaluation Unit, Bologna, Italy

*Simona Di Mario, SaPeRiDoc, Primary health care, general medicine, planning and development of health services, Regional health authority of Emilia-Romagna, Bologna, Italy. sdimario@regione.emilia-romagna.it.

Publication History

  1. Publication Status: New search for studies and content updated (no change to conclusions)
  2. Published Online: 28 FEB 2013

SEARCH

 

Background

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms

Congenital toxoplasmosis is a rare (NSC 2001) but potentially severe parasitic infection that can lead to intrauterine death or stillbirth, malformation, mental retardation, deafness and blindness of the infected infant (Montoya 2004). Incidence of congenital toxoplasmosis varies from one to 10 per 10,000 live children in Western countries (Gilbert 1999; Schmidt 2006; Signorell 2006), to 16 per 1000 in Brazil (Reis 1999). The infection is caused by Toxoplasma gondii (T. gondii). T. gondii is one of the most common infectious pathogenic animal parasites of man, belonging to the phylum apicomplexa group (Montoya 2004). Other members of this phylum include known human pathogens such as Plasmodium (malaria) and Cryptosporidium. It is acquired by ingesting oocysts excreted by cats, contaminated soil or water, or by eating the undercooked meat of infected animals, which contain tissue cysts (Gilbert 2002; Montoya 2004). Most cases of toxoplasmosis infection are asymptomatic and self-limited except for congenital infection and immunocompromised patients (Montoya 2004); hence many cases remain undiagnosed. The incubation period of acquired infection is estimated to be within the range of four to 21 days (seven days on average) (Rorman 2006). Serological surveys demonstrate that worldwide exposure to T. gondii is high (30% in USA and 50% to 80% in Europe) (Rorman 2006). The susceptibility of pregnant women (that is the rate of seronegative pregnant women) to toxoplasmosis varies between countries. It is up to 90% in northern Europe, where T. gondii is not so common (Allain 1998; Gilbert 2002). When infection does occur during pregnancy, T. gondii can be transmitted from the mother to the fetus (vertical transmission) and can lead to congenital toxoplasmosis. Multiple factors are associated with the occurrence of congenital toxoplasmosis infection, including route of transmission, climate, cultural behavior, eating habits and hygenic standards (Rorman 2006). The probability of transmission of the parasite to the fetus varies according to the gestational age and the risk is greater during the third trimester (from 5% at 12 weeks to 80% just before delivery) (Dunn 1999). Conversely, the severity of the condition, that is the risk of the fetus developing major clinical signs, decreases with increasing gestational age (from 60% at 12 weeks to 5% just before delivery) (Dunn 1999). Clinical features include hydrocephalus (excessive accumulation of cerebrospinal fluid within the cranium), microcephaly (abnormal smallness of the head, usually associated with mental retardation), deafness, cerebral calcifications, seizures and psychomotor retardation. Signs of a systemic infection may also be present at birth, including fever, rash, and enlargement of liver and spleen. Fetal infection can cause inflammatory lesions of the retina and choroids that can lead to visual impairment. Moreover, it can cause lesions of the brain leading to mental damage; more rarely, the infection can cause the death of the fetus or the newborn (Gilbert 2002; Montoya 2004; NSC 2001). Severe damage in infancy occurs in 5% of congenital toxoplasmosis cases, while intracranial or ocular lesions are observed in 20% to 30% of cases by three years of age (Gilbert 2001). Although there is no consensus on the most appropriate screening or treatment for congenital toxoplasmosis, three possible approaches have been proposed: prenatal screening, neonatal screening and primary prevention (Gilbert 2002).

 

Prenatal screening

Prenatal screening (secondary prevention) is offered in some European countries, for example, France, Switzerland, Germany, Austria and Italy where the incidence of T. gondii maternal infection is more frequent, and is based on the timely detection of the mother's infection by a serum test for toxoplasma Immunoglobulin G (IgG) and Immunoglobulin M (IgM) (NSC 2001). If the first prenatal test shows signs of recent infection or a seroconversion is detected during pregnancy, a confirmatory test is required before starting treatment with spiramycin or pyrimethamine-sulfadoxine, or both (Foulon 1999a; Gilbert 2002; Montoya 2004). Diagnosis of fetal infection is performed by amniocentesis, which is known to be associated with a 1% risk of miscarriage (Alfirevic 2003) and testing of the amniotic fluid for the detection of the parasite or, most recently, of toxoplasma DNA by polymerase chain reaction (PCR) technique. Congenital toxoplasmosis can also be diagnosed by cordocentesis, that consists of drawing fetal blood from the umbilical cord, and the detection of the parasite or specific immunoglobulin (IgM and IgA) in the fetal blood, but the risk of complications due to the procedure is higher (Bader 1997; Foulon 1999b; Gilbert 2002). If fetal infection is confirmed, the parents can decide either to terminate the pregnancy or to opt for drug treatment. Prenatal screening, although advocated by some as essential for reducing congenital toxoplasmosis (Boyer 2005), has several limitations: false-positive toxoplasma IgM results are common, false-positive toxoplasma IgG are less common but also possible (Liesenfeld 1997; Montoya 2004); moreover, the rate of false-positive test results can increase notably in settings where local prevalence of the infection is lower; there can be organizational problems or problems of acceptability due to the need to repeat the serum test every four to six weeks in seronegative women (Bader 1997); there is no evidence that antenatal treatment is effective in reducing transmission to the fetus nor in improving neonatal outcomes or reducing functional impairment in later childhood (Gilbert 2003; Peyron 1999; SYROCOT 2007); there are problems concerning the accuracy of the diagnostic test for fetal infection, particularly the lack of a standardized technique for PCR (Chabbert 2004; Foulon 1999b; Thalib 2005). Finally, this strategy causes additional fetal losses of healthy fetuses due to amniocentesis and to elective terminations of pregnancy. It has been estimated that the number of additional losses necessary to prevent one additional case of toxoplasmosis can be as high as 18.5 in cases of universal screening in a setting with a low incidence of T. gondii maternal infection, such as the USA (Bader 1997).

 

Neonatal screening

Neonatal screening (tertiary prevention), adopted in Poland, Denmark and some areas of the USA (NSC 2001), consists of the diagnosis of newborn infection through detection of toxoplasma specific IgM on Guthrie card blood spots. In fact, up to 90% of infected infants are asymptomatic at birth and will show clinical symptoms only in later life (Gilbert 2001; Wilson 1980). Current guidelines suggest that infected infants should receive treatment with pyrimethamine and sulfadiazine for up to one year, regardless of symptoms (Gilbert 2002). Even if this strategy is technically feasible and less costly than prenatal screening, it has been proven to have a low sensitivity, even when the test is performed on serum samples, which are more valid than the test on filter paper blood samples currently used: neonatal screening is not able to detect almost half of all infected infants (Gilbert 2007). Moreover, there is no evidence that treating the infected children has any effect (Gilbert 2002; Lebech 1999). Finally, this approach is ineffective on irreversible damage already present at birth. Considering such limitations, neonatal screening should be adopted only in places where other options are not available; the implications of such a policy should be fully discussed with the parents of the tested newborn.

 

Primary prevention

Primary prevention can involve the whole population by educating the general public and filtering water, and veterinary public health interventions (such as labeling to indicate toxoplasma-free meat and improved farm hygiene to reduce animal infection). This will reduce the protozoan circulation and could be an option but up to now there is not enough research to determine the feasibility and efficacy of this approach (Gilbert 2002; NSC 2001). Another possibility is primary prevention based on prenatal education of pregnant women or women of reproductive age to avoid toxoplasmosis in pregnancy (Gilbert 2002). In fact, sources and risk factors for contracting toxoplasmosis are well known (Cook 2000) and can be avoided by adopting simple behavioral measures such as not eating raw or insufficiently cooked meat, washing hands thoroughly after handling raw meat and after gardening, avoiding contact with cats' faeces (directly or indirectly through the soil, or possibly contaminated raw vegetables or fruits) (Cook 2000; Gilbert 2002). Nevertheless, pregnant women are often unaware of risk factors for congenital toxoplasmosis (Ferguson 2011). Primary prevention based on prenatal education, if proven to be effective, could be a good strategy to reduce congenital toxoplasmosis, since it will not involve any of the problems linked to secondary and tertiary prevention strategies discussed above.

Readers may wish to refer to the following Cochrane systematic review for further information about toxoplasmosis in pregnancy: 'Treatments for toxoplasmosis in pregnancy' (Peyron 1999).

 

Objectives

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms

The primary objectives of this review were to assess the efficacy of prenatal education to reduce the rate of:

  1. new cases of congenital toxoplasmosis;
  2. toxoplasmosis seroconversion during pregnancy.

Secondary objectives were to assess the efficacy of prenatal education to increase the rate of:

  1. pregnant women's knowledge of risk factors for acquiring toxoplasmosis infection;
  2. pregnant women's awareness of the importance of avoiding toxoplasmosis infection during pregnancy;
  3. pregnant women's behavior with respect to avoidance of risk factors for toxoplasmosis infection during pregnancy.

 

Methods

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms
 

Criteria for considering studies for this review

 

Types of studies

Randomized and quasi-randomized controlled trials evaluating any kind of prenatal educational intervention dealing with toxoplasmosis infection in pregnancy, and how to avoid it, were assessed for inclusion. Studies where the control group included an alternative intervention or no intervention were also considered for inclusion. Studies where the unit of randomization was a group of women (cluster-randomization) were assessed for inclusion and analyzed as a separate group. Interventions, exclusively focused on toxoplasmosis or interventions not exclusively focused on toxoplasmosis infection but where toxoplasmosis was included among a series of different topics, were also eligible for inclusion.

 

Types of participants

Trials of women of reproductive age, irrespective of their pregnant status were included. Since a screening policy for toxoplasmosis infection is not universally adopted, studies including women irrespective of their toxoplasmosis seropositive status were included.

 

Types of interventions

Any kind of prenatal education on toxoplasmosis infection during pregnancy. Prenatal educational interventions could include: antenatal classes provided to pregnant women, distribution of leaflets to pregnant women or to women of reproductive age irrespective of their pregnant status, one-to-one or group counseling from different professionals (nurses, midwives, obstetricians and gynecologists, social workers, counselors, teachers, trained lay people, etc), educational intervention in schools, mass-media campaign and others.

 

Types of outcome measures

 

Primary outcomes

  1. Rate of congenital toxoplasmosis, defined by persistence of specific IgG antibodies beyond 11 months of age (Lebech 1996).
  2. Rate of toxoplasmosis seroconversion in pregnant women, defined by:

  • an increase in specific IgG from paired sera in pregnant woman previously seronegative;
  • a rising IgG titre, low IgG avidity, IgA antibodies, or a combination of these in pregnant women who were IgG and IgM positive at their first prenatal test (Gilbert 2002).

 

Secondary outcomes

  1. Pregnant women's knowledge of risk factors for acquiring toxoplasmosis infection as objectively measured (quantitative score) through specific questionnaire.
  2. Pregnant women's awareness of the importance of avoiding toxoplasmosis infection during pregnancy as objectively measured (quantitative score) through specific questionnaire.
  3. Pregnant women's behavior with respect to the avoidance of risk factors for toxoplasmosis infection during pregnancy as objectively measured (quantitative score) through specific questionnaire.

 

Search methods for identification of studies

 

Electronic searches

We searched the Cochrane Pregnancy and Childbirth Group’s Trials Register by contacting the Trials Search Co-ordinator (15 January 2012).

The Cochrane Pregnancy and Childbirth Group’s Trials Register is maintained by the Trials Search Co-ordinator and contains trials identified from:

  1. monthly searches of the Cochrane Central Register of Controlled Trials (CENTRAL);
  2. weekly searches of MEDLINE;
  3. weekly searches of EMBASE;
  4. handsearches of 30 journals and the proceedings of major conferences;
  5. weekly current awareness alerts for a further 44 journals plus monthly BioMed Central email alerts.

Details of the search strategies for CENTRAL, MEDLINE and EMBASE, the list of handsearched journals and conference proceedings, and the list of journals reviewed via the current awareness service can be found in the ‘Specialized Register’ section within the editorial information about the Cochrane Pregnancy and Childbirth Group.

Trials identified through the searching activities described above are each assigned to a review topic (or topics). The Trials Search Co-ordinator searches the register for each review using the topic list rather than keywords. 

In addition, we searched PubMed (1966 to 15 January 2012), EMBASE (Embase.com) (1980 to 15 January 2012), CINAHL (EBSCO) (1982 to 15 January 2012), LILACS - Latin American and Caribbean Health Science Literature (1982 to 15 January 2012), and IMEMR - Eastern Mediterranean Region Index Medicus (1984 to 15 January 2012). See Appendix 1 for search strategy.

 

Searching other resources

We searched the reference lists of relevant papers, reviews and websites and contacted researchers working in the field for information on any relevant studies and for any additional published or unpublished studies.

We did not apply any language restrictions.

 

Data collection and analysis

For the methods used in the previous version of this review, see Appendix 2.

For this update we used the following methods. Since one of the two trials included did not provide raw data, it was not possible to pool the data. Single trial results are presented in Effects of interventions paragraph. Baseline general data for each study are presented in tables (see Characteristics of included studies).

Additional methods for data collection and analysis to be used in subsequent updates are provided in Appendix 3.

 

Selection of studies

Two review authors independently assessed for inclusion all the potential studies we identified as a result of the search strategy. We resolved any disagreement through discussion.

 

Data extraction and management

We designed a form to extract data. For eligible studies, two review authors extracted the data using the agreed form. We resolved discrepancies through discussion. In future updates, as more data become available, we will enter data into Review Manager software (RevMan 2011) and check it for accuracy.

When information regarding any of the above was unclear, we attempted to contact authors of the original reports to provide further details.

 

Assessment of risk of bias in included studies

Two review authors independently assessed risk of bias for each study using the criteria outlined in the Cochrane Handbook for Systematic Reviews of Interventions (Higgins 2011). We resolved any disagreement by discussion.

 

(1) Random sequence generation (checking for possible selection bias)

We described for each included study the method used to generate the allocation sequence in sufficient detail to allow an assessment of whether it should produce comparable groups.

We assessed the method as:

  • low risk of bias (any truly random process, e.g. random number table; computer random number generator);
  • high risk of bias (any non-random process, e.g. odd or even date of birth; hospital or clinic record number);
  • unclear risk of bias.   

 

 (2) Allocation concealment (checking for possible selection bias)

We described for each included study the method used to conceal allocation to interventions prior to assignment and assess whether intervention allocation could have been foreseen in advance of, or during recruitment, or changed after assignment.

We assessed the methods as:

  • low risk of bias (e.g. telephone or central randomization; consecutively numbered sealed opaque envelopes);
  • high risk of bias (open random allocation; unsealed or non-opaque envelopes, alternation; date of birth);
  • unclear risk of bias.   

 

(3.1) Blinding of participants and personnel (checking for possible performance bias)

We described for each included study the methods used, if any, to blind study participants and personnel from knowledge of which intervention a participant received. We considered studies to be at low risk of bias if they were blinded, or if we judged that the lack of blinding would be unlikely to affect results. We assessed blinding separately for different outcomes or classes of outcomes.

We assessed the methods as:

  • low, high or unclear risk of bias for participants;
  • low, high or unclear risk of bias for personnel;

 

(3.2) Blinding of outcome assessment (checking for possible detection bias)

We described for each included study the methods used, if any, to blind outcome assessors from knowledge of which intervention a participant received. We assessed blinding separately for different outcomes or classes of outcomes.

We assessed the methods used to blind outcome assessment as:

  • low, high or unclear risk of bias.

 

(4) Incomplete outcome data (checking for possible attrition bias due to the amount, nature and handling of incomplete outcome data)

We described for each included study, and for each outcome or class of outcomes, the completeness of data including attrition and exclusions from the analysis. We state whether attrition and exclusions were reported and the numbers included in the analysis at each stage (compared with the total randomized participants), reasons for attrition or exclusion where reported, and whether missing data were balanced across groups or were related to outcomes.

We assessed methods as:

  • low risk of bias (e.g. no missing outcome data; missing outcome data balanced across groups);
  • high risk of bias (e.g. numbers or reasons for missing data imbalanced across groups; ‘as treated’ analysis done with substantial departure of intervention received from that assigned at randomization);
  • unclear risk of bias.

 

(5) Selective reporting (checking for reporting bias)

We described for each included study how we investigated the possibility of selective outcome reporting bias and what we found.

We assessed the methods as:

  • low risk of bias (where it is clear that all of the study’s pre-specified outcomes and all expected outcomes of interest to the review have been reported);
  • high risk of bias (where not all the study’s pre-specified outcomes have been reported; one or more reported primary outcomes were not pre-specified; outcomes of interest are reported incompletely and so cannot be used; study fails to include results of a key outcome that would have been expected to have been reported);
  • unclear risk of bias.

 

(6) Other bias (checking for bias due to problems not covered by 1 to 5 above)

We described for each included study any important concerns we have about other possible sources of bias.

We assessed whether each study was free of other problems that could put it at risk of bias:

  • low risk of other bias;
  • high risk of other bias;
  • unclear whether there is risk of other bias.

 

(7) Overall risk of bias

We made explicit judgements about whether studies were at high risk of bias, according to the criteria given in the Cochrane Handbook for Systematic Reviews of Interventions (Higgins 2011). With reference to (1) to (6) above, we assessed the likely magnitude and direction of the bias and whether we considered it likely to impact on the findings. We explored the impact of the level of bias through undertaking sensitivity analyses - see 'Sensitivity analysis'. 

 

Results

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms
 

Description of studies

See: Characteristics of included studies; Characteristics of excluded studies.

Nine-hundred and twenty-five studies met the initial criteria for hard copy scrutiny. Five studies (corresponding to nine publications) met the predetermined baseline criteria of assessing an educational intervention for toxoplasmosis prevention. Two studies (involving 5455 women) have been included and three studies have been excluded. See Figure 1 for diagram of the studies selection.

 FigureFigure 1. Study flow diagram.

 

Included studies

The first study compared two randomly allocated groups of women and was therefore included in the review (Carter 1989). The study was conducted in Ontario (Canada) and involved 432 pregnant women attending early prenatal classes in six centers. It was a cluster-randomized trial, that is, a trial where groups rather than individuals are randomized between or among comparator interventions; in this case, the units of randomization were the prenatal classes: 26 prenatal classes were randomly assigned to the intervention and 26 prenatal classes were assigned to control intervention (usual prenatal classes). A three-page handout was prepared along with a display poster and resource materials for teachers. Prenatal class instructors received one-hour basic training on toxoplasmosis prevention. The intervention group women were offered a 10-minute presentation focused on toxoplasmosis prevention during the first prenatal class. The contents of the intervention focused on cats, food and personal hygiene. The second study was a cluster-randomized trial conducted in France (Wallon 2006). Women attending prenatal clinics in the area of Lyon were enrolled if tested seronegative for toxoplasma antibodies. The unit of randomization were the cities. Physicians in experimental cities provided women with a 20-page brochure containing four pages of information of toxoplasmosis plus an audiotape containing a conversation between a physician and her patient on issued relevant to pregnancy, including questions on toxoplasmosis. Women attending prenatal clinics in control cities received usual care. Knowledge and behavior were assessed through a questionnaire administered at baseline (usually during the third and fourth month of gestation) and at follow-up (after delivery). Only women who filled both questionnaires (2790 out of 5023) were included in the multivariate analysis to identify any association between the intervention and change in knowledge and behavior.

 

Excluded studies

The remaining three studies were surveys conducted at the population level, without a control group (before and after studies) and were, therefore, excluded from the review as they were not randomized controlled trials. The details of the three studies are shown in  Table 1. One study was from Belgium (Breugelmans 2004), one from Poland (Pawlowski 2001), and one from Cuba (Molé 1992). In the Breugelmans study the intervention changed over time: the first intervention adopted (from 1983 to 1990) consisted of providing pregnant women with a list of recommended hygiene measures to avoid toxoplasma infection during pregnancy; thereafter (from 1991 to 2001) a leaflet containing information on congenital toxoplasmosis and how to avoid it was given to all pregnant women in addition to the list of recommendations and was assessed for effectiveness. Seroconvertion rate during pregnancy in the intervention period was compared with the seroconversion rate in the baseline period, when no intervention on toxoplasmosis prevention was in place (from 1979 to 1982) (Breugelmans 2004). The Pawlowski 2001 study used a multifaceted intervention including providing information to pregnant women, refresher training for health professionals, media campaigns, and the training of biology teachers in secondary schools, over six years and their effectiveness was assessed. It was impossible to obtain the full text of the study conducted in Cuba (Molé 1992): data retrieved from the abstract indicate that an educational intervention about how to avoid toxoplasmosis infection during pregnancy was delivered to seronegative pregnant women. All pregnant women were enrolled at their first prenatal visit. The number of women included in the surveys ranged from 1246 to 16,541. The Breugelmans 2004 study contained data previously published in Foulon (Foulon 1988; Foulon 1994).

 

Risk of bias in included studies

The Canadian trial (Carter 1989), was a cluster-randomized trial of low quality (Hahn 2005; Puffer 2003). The study reported that the groups were randomized but the randomization method was not specified. Nevertheless, allocation bias of the cluster is unlikely: the six centers provided almost all of the prenatal education available in that jurisdictional area; the study only lasted six months; an equal number of classes in each center received the experimental and the control intervention; authors stated that experimental and control women did not differ for demographic characteristics (even though a table reporting baseline data of the two groups was not provided), thus there is no strong reason to suspect that women attending prenatal classes in one period of time differ significantly from women attending prenatal classes in another period of time. Losses to follow-up at the level of women participating to prenatal classes were 34% (432 women completed the pretest questionnaire and 285 completed the post-test questionnaire): women in experimental group were more likely to be lost at follow-up than women in control group, therefore attrition bias can not be excluded (Puffer 2003). Outcome measures referred to changes in behavior occurring between pre-test (usually in the first-second term of pregnancy) and post-test questionnaire (in the third term of pregnancy) in respect of hygiene measures to avoid toxoplasmosis. Since outcome measures were self-reported, information bias can not be totally excluded, even if women were blinded to the objective of the study. Finally, since the prenatal class instructors of the experimental and the control group were the same, it is not possible to exclude some contamination, even if such contaminations are usually not an issue in cluster trials (Torgerson 2001), and in any case, it would have acted in the sense of reducing the effect. The total sample, considering the unit of randomization, was low (26 prenatal classes in the intervention group and 26 prenatal classes in the control group). It is not clear from the paper if a statistical analysis was conducted to take into account the effect of intracluster correlation. The authors did not report raw data (number or proportion): only P value for differences were reported. We also contacted the authors for the original data but have not yet received a reply. The second trial included (Wallon 2006) was also a cluster-randomized trial of low quality: randomization method was not specified. The study, first used for a master thesis, was published in a short form as a poster, and thereafter included in a systematic review. In neither of the publications was the statistical plan of analysis described. Overall losses to follow-up were 44.5%: women in the control group were more likely to be lost at follow-up (52% were lost) than women in intervention group (40% were lost), therefore, attrition bias can not be excluded (Puffer 2003). Outcome measures referred to changes in behavior occurring between pre-test (usually in the third and fourth month of pregnancy) and post-test questionnaire (at delivery) in respect of hygiene measures to avoid toxoplasmosis. Since outcome measures were self-reported, information bias can not be totally excluded, even if women were blinded to the objective of the study.

 

Effects of interventions

Since the two included trials reported measure of effectiveness of the intervention assessed in a non comparable way, meta-analysis of the results was not possible.

The first trial included in the review (Carter 1989) reported the following changes in behavior in the intervention group:

  • pet hygiene behavior: intervention classes reported to behave significantly better than the control class (P value reported < 0.05);
  • food hygiene behavior: intervention classes reported to behave significantly better than the control class with respect to cooking roast beef (P value reported < 0.05) and hamburgers (P value reported < 0.01); remaining items were already good at the pre-test;
  • personal hygiene behavior intervention classes reported to behave significantly better than the control class only in the subgroup of women who had professional occupations (P value reported < 0.05); remaining professional groups and other items considered were already good at the pre-test.

Only 5% of the women in the intervention group recall having obtained specific information on toxoplasmosis prevention during prenatal classes.

The second trial included in the review (Wallon 2006) reported the following results:

  • seroconvertions for toxoplasmosis detected during the study did not differ between groups: there were 13 cases out of 2591 pregnant women (0.5%) in the intervention group and four cases out of 1358 pregnant women (0.3%) in the control group (P = 0.35);
  • prenatal education on congenital toxoplasmosis was not significantly associated to the outcome "no consumption of undercooked meat of any type" (multiple logistic regression, odds ratio (OR) 1.21; 95% confidence interval (CI) 0.98, 1.50);
  • prenatal education on congenital toxoplasmosis was not significantly associated to the outcome "handwashing after contact with transmission factor and before meals" (multiple logistic regression, OR 1.01; 95% CI 0.83, 1.22);
  • baseline behaviors concerning toxoplasmosis, smoking and alcohol consumption were significantly associated with both the outcomes measured, after controlling for baseline knowledge.

 

Discussion

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms

Two cluster-randomized trials on primary prevention of congenital toxoplasmosis suggest that providing specific information during antenatal classes or prenatal visits about toxoplasmosis infection and how to avoid it can improve pregnant women's behavior (Carter 1989; Wallon 2006), but the overall quality of the trials was poor.

In addition, three observational studies consistently suggest that prenatal education might have a positive impact on reducing congenital toxoplasmosis (Breugelmans 2004; Molé 1992; Pawlowski 2001).

Giving the scarcity of evidence supporting the implementation of antenatal classes for congenital toxoplasmosis, and considering the current lack of evidence that alternative interventions such as screening and early treatment of infected pregnant women can reduce the risk of congenital toxoplasmosis, further research to quantify the impact of different educational interventions is needed.

 

Authors' conclusions

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms

 

Implications for practice

Evidence supporting prenatal education for preventing congenital toxoplasmosis is sparse and of low quality. Prenatal education could have a positive effect in terms of improving women's behavior and reducing seroconversion during pregnancy but strong evidence is still lacking. In settings where prenatal educative interventions are already in place, it could be beneficial to consider offering a specific session on how to avoid toxoplasmosis infection and provide printed materials that are informative.

A good surveillance system should be in place whenever a prenatal education activity is implemented to monitor the prevalence of seropositivity among pregnant women and to detect cases of congenital toxoplasmosis among the offspring of women who seroconverted during pregnancy.

 
Implications for research

Given the limited evidence supporting prenatal education for congenital toxoplasmosis prevention, further randomized controlled trials are needed. Given the nature of the intervention, those trials would most probably be cluster-randomized trials, that is a trial were groups rather than individuals are randomized between or among comparator interventions. The studies should focus on assessing the impact of different sets of intervention. The adequate sample size to detect a reduction of the incidence of congenital toxoplasmosis can be calculated considering at least two possible scenarios depending on the background incidence and hypothesized effect of intervention. In countries with high incidence rate like Brazil (16/1000) (Reis 1999) and in countries with low incidence rate like western Europe (10/10,000) (Gilbert 1999), predicting a 50% reduction of incidence in the intervention arm of the trial (Breugelmans 2004), considering a 95% confidence level and a 80% study power, and after doubling the sample to take in account the design effect of the cluster-randomized trial, the needed sample will be (EpiInfo 6):

  • countries with high incidence like Brazil: 6300 women per arm;
  • countries with low incidence like western Europe: 102,000 women per arm.

As results from this raw calculation, only large studies will be able to detect a difference in terms of incidence of congenital toxoplasmosis; therefore, careful consideration should be given in valuing the balance between benefits and costs of such trials. Trials assessing the effect of a multilevel prenatal educational intervention also including toxoplasmosis prevention among others, and measuring the change in behavior or better pregnancy outcome as a composite outcome, might be more practical and preferable. Finally, we also suggest that in planning such trials, a checklist for good quality reporting of cluster-randomized trials, for example, a modified Consolidated Standards Of Reporting Trials (CONSORT) (Campbell 2004), should be followed to ensure better quality and to provide valuable information.

 

Acknowledgements

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms

We acknowledge Dr Chiara Bassi, CeVEAS, Modena, for designing and running the search strategy, and Dr Sara Balduzzi, Modena and Reggio Emilia University, for providing inputs and comments on the updated version of the review.

 

Data and analyses

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms

This review has no analyses.

 

Appendices

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms
 

Appendix 1. Search strategy

 
Search strategies written and run by authors:

 
PubMed (1966 to 15 January 2012):

#1. toxoplasm*
#2. 'toxoplasma'/exp
#3. 'toxoplasmosis'/exp
#4. #1 OR #2 OR #3
#5. neonat*
#6. antenat*
#7. infant*
#8. ('baby'/exp OR 'baby')
#9. babies
#10. foet*
#11. fetus
#12. fetal*
#13. p?ediatr*
#14. prenat*
#15. 'infant'/exp
#16. 'fetus'/exp
#17. 'pediatrics'/exp
#18. OR/ #5-#17
#19. #4 AND #18
#20.'mass media'/exp OR 'mass media'
#21. communication*
#22. multimedia*
#23. 'multi media'
#24. 'multimedia'/exp
#25. 'mass communication'
#26. ('audiovisual equipment'/exp OR 'audiovisual equipment')
#27. ('patient information'/exp OR 'patient information')
#28. ('visual information'/exp OR 'visual information')
#29. ('radio'/exp OR 'radio')
#30. ('television'/exp OR 'television')
#31. leaflet*
#32. poster*
#33. pamphlet*
#34. 'print media'
#35. 'printed media'
#36. 'broadcast'
#37. film*
#38. ('telecommunication'/exp OR telecommunication*)
#39. counsel*
#40. educat*
#41. empower*
#42. knowledge*
#43. skill*
#44. 'public health'/exp
#45. 'preventive medicine'/exp
#46. 'preventive health service'/exp
#47. 'primary health care'/exp
#48. 'health care delivery'/exp
#49. 'patient attitude'/exp
#50. 'primary prevention'/exp
#51. 'health promotion'/exp
#52. 'health education'/exp
#53. 'patient education'/exp
#54. 'education'/exp
#55. 'attitude'/exp
#56. 'cognition'/exp
#57. 'health behavior'/exp
#58. 'decision making'/exp
#59 OR/#20-#58
#60 #19 AND #59

 
EMBASE (Embase.com) (1980 to 15 January 2012)

#1. toxoplasm*
#2. 'toxoplasma'/exp
#3. 'toxoplasmosis'/exp
#4. #1 OR #2 OR #3
#5. neonat*
#6. antenat*
#7. infant*
#8. ('baby'/exp OR 'baby')
#9. babies
#10. foet*
#11. fetus
#12. fetal*
#13. p?ediatr*
#14. prenat*
#15. 'infant'/exp
#16. 'fetus'/exp
#17. 'pediatrics'/exp
#18. OR/ #5-#17
#19. #4 AND #18
#20.'mass medium'/exp OR 'mass media'
#21. communication*
#22. multimedia*
#23. 'multi media'
#24. 'mass communication'
#25. ('audiovisual equipment'/exp OR 'audiovisual equipment')
#26. ('patient information'/exp OR 'patient information')
#27. ('visual information'/exp OR 'visual information')
#28. radio
#29. ('television'/exp OR 'television')
#30. leaflet*
#31. poster*
#32. pamphlet*
#33. 'print media'
#34. 'printed media'
#35. 'broadcast'
#36. film*
#37. ('telecommunication'/exp OR telecommunication*)
#38. counsel*
#39. educat*
#40. empower*
#41. knowledge*
#42. skill*
#43. 'public health'/exp
#44. 'preventive medicine'/exp
#45. 'preventive health service'/exp
#46. 'primary health care'/exp
#47. 'health care delivery'/exp
#48. 'patient attitude'/exp
#49. 'primary prevention'/exp
#50. 'health promotion'/exp
#51. 'health education'/exp
#52. 'patient education'/exp
#53. 'education'/exp
#54. 'attitude'/exp
#55. 'cognition'/exp
#56. 'health behavior'/exp
#57. 'decision making'/exp
#58 OR/#20-#57
#59 #19 AND #58

 
CINAHL (via EBSCO) (1982 to 15 January 2012)

#1. toxoplasm*
#2. MH 'toxoplasmosis'
#3. #1 OR #2
#4. neonat*
#5. antenat*
#6. infant*
#7. baby
#8. babies
#9. foet*
#10. fetus
#11. fetal*
#12. p?ediatr*
#13. prenat*
#14. MH 'infant'
#15. MH 'fetus'
#16. MH 'pediatrics'
#17. OR/ #4-#16
#18. #3 AND #17
#19. MH 'communication media' OR 'mass media'
#20. communication*
#21. multimedia*
#22. 'multi media'
#23. 'mass communication'
#24. MH 'audiovisuals' OR 'audiovisual equipment'
#25. 'patient information'
#26. 'visual information'
#27. MH 'radio' OR 'radio'
#28. MH 'television' OR 'television'
#29. leaflet*
#30. poster*
#31. pamphlet*
#32. 'print media'
#33. 'printed media'
#34. 'broadcast'
#35. film*
#36. MH 'telecommunications' OR telecommunication*
#37. counsel*
#38. educat*
#39. empower*
#40. knowledge*
#41. skill*
#42. 'public health'/exp
#43. MH 'preventive health care'
#44. MH 'primary health care'
#45. MH 'health care delivery'
#46. MH 'patient attitudes'
#47. MH 'primary prevention'
#48. MH 'health services needs and demand’
#49. MH 'health education'
#50. MH 'patient education'
#51. MH 'education’
#52. MH 'attitude'
#53. MH 'cognition'
#54. MH 'health behavior'
#55. MH 'decision making'
#56 OR/#19-#55
#67 #18 AND #56

 
LILACS (1982 to 15 January 2012) and IMEMR (1984 to 15 January 2012):

#1 congenital toxoplasmosis

 

Appendix 2. Methods used to assess trials included in previous versions of this review

The following methods were used to assess Carter 1989 in the initial version of this review.

 

Studies selection and quality assessment

Titles and abstract of the identified trials were selected in an independent and blinded way for inclusion in the review by two review authors. The methodological quality of included trials was assessed according to the criteria in the Cochrane Handbook for Systematic Reviews of Interventions (Higgins 2011), with a grade allocated to each trial on the basis of allocation concealment: A (adequate), B (unclear), C (clearly inadequate). Details regarding randomization method, completeness of follow-up, blinding of outcome measures were documented for all trials using a standard checklist. Cluster-randomized and quasi-randomized designs, such as alternate allocation and use of record numbers were included. Differences of opinion regarding trials for inclusion were solved through discussion. Data extraction was performed independently by two authors using prepared data extraction forms.

 

Appendix 3. Data collection and analysis methods to be used in future updates

 

Measures of treatment effect  

 

Dichotomous data

For dichotomous data, we will present results as summary risk ratio with 95% confidence intervals. 

 

Continuous data

For continuous data, we will use the mean difference if outcomes are measured in the same way between trials. We will use the standardized mean difference to combine trials that measure the same outcome, but use different methods.  

 

Unit of analysis issues  

 

Cluster-randomized trials

If we identify any cluster-randomized trials, we will include them in the analyses along with individually-randomized trials. We will adjust their sample sizes using the methods described in the Cochrane Handbook for Systematic Reviews of Intervention [Section 16.3.4] using an estimate of the intracluster correlation co-efficient (ICC) derived from similar trial or from a study of a similar population. We will also conduct sensitivity analyses to investigate the effect of variation in the ICC. If we identify both cluster-randomized trials and individually-randomized trials, we plan to synthesize the relevant information. We will consider it reasonable to combine the results from both if there is little heterogeneity between the study designs and the interaction between the effect of intervention and the choice of randomization unit is considered to be unlikely.

We will also acknowledge heterogeneity in the randomization unit and perform a subgroup analysis to investigate the effects of the randomization unit.

 

Dealing with missing data  

For included studies, we will note levels of attrition. We will explore the impact of including studies with high levels of missing data in the overall assessment of treatment effect by using sensitivity analysis.

For all outcomes, we will carry out analyses, as far as possible, on an intention-to-treat basis, i.e. we will attempt to include all participants randomized to each group in the analyses, and all participants will be analyzed in the group to which they were allocated, regardless of whether or not they received the allocated intervention. The denominator for each outcome in each trial will be the number randomized minus any participants whose outcomes are known to be missing.

 

Assessment of heterogeneity  

We will assess statistical heterogeneity in each meta-analysis using the T², I² and Chi² statistics. We will regard heterogeneity as substantial if I² is greater than 30% and either T² is greater than zero, or there is a low P value (less than 0.10) in the Chi² test for heterogeneity. 

 

Assessment of reporting biases  

If there are 10 or more studies in the meta-analysis we will investigate reporting biases (such as publication bias) using funnel plots. We will assess funnel plot asymmetry visually, and use formal tests for funnel plot asymmetry. For continuous outcomes we will use the test proposed by Egger 1997, and for dichotomous outcomes we will use the test proposed by Harbord 2006. If asymmetry is detected in any of these tests or is suggested by a visual assessment, we will perform exploratory analyses to investigate it.

 

Data synthesis  

We will carry out statistical analysis using the Review Manager software (RevMan 2011). We will use fixed-effect meta-analysis for combining data where it is reasonable to assume that studies are estimating the same underlying treatment effect: i.e. where trials are examining the same intervention, and the trials’ populations and methods are judged sufficiently similar. If there is clinical heterogeneity sufficient to expect that the underlying treatment effects differ between trials, or if substantial statistical heterogeneity is detected, we will use random-effects meta-analysis to produce an overall summary if an average treatment effect across trials is considered clinically meaningful. The random-effects summary will be treated as the average range of possible treatment effects and we will discuss the clinical implications of treatment effects differing between trials. If the average treatment effect is not clinically meaningful, we will not combine trials.

If we use random-effects analyses, the results will be presented as the average treatment effect with 95% confidence intervals, and the estimates of  T² and I².

 

Subgroup analysis and investigation of heterogeneity  

If we identify substantial heterogeneity, we will investigate it using subgroup analyses. We will consider whether an overall summary is meaningful, and if it is, use random-effects analysis to produce it.

We plan to carry out all or part of the following subgroup analyses depending on the characteristics of the studies that we will identify:

  1. background risk of infection (studies conducted in area with low incidence rate of congenital toxoplasmosis and studies conducted in areas with high incidence rate of congenital toxoplasmosis);    
  2. health professionals providing the education (counselors, gynecologists, midwives, etc);
  3. information strategy used (printed materials, face-to-face information, class groups, videotapes, etc).

Subgroup analysis will be restricted to primary outcomes.

We will assess subgroup differences by interaction tests available within RevMan (RevMan 2011). We will report the results of subgroup analyses quoting the χ2 statistic and P value, and the interaction test I² value.

 

Sensitivity analysis

A sensitivity analysis based on study quality (high quality and low quality studies based on assessment of risk of bias) will be conducted.

 

What's new

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms

Last assessed as up-to-date: 15 May 2012.


DateEventDescription

15 January 2012New search has been performedSearch updated. No new studies identified.

One study (Wallon 2006), previously classified as pending has been included. This review now contains two included studies (involving a total of 5455 women).

The methods have been updated.

15 January 2012New citation required but conclusions have not changedThis review has been updated. The addition of one more included study has not changed the results and conclusions.



 

History

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms

Protocol first published: Issue 4, 2006
Review first published: Issue 1, 2009


DateEventDescription

16 January 2008AmendedConverted to new review format.



 

Contributions of authors

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms

First version of the review: Simona Di Mario (SDM), Vittorio Basevi (VB) and Daniela Spettoli (DS) were responsible for the conception of the study. SDM, DS, Carlo Gagliotti (CG) and Gianfranco Gori selected the studies and assessed the quality. SDM, DS and CG collected and analyzed the data. VB, Nicola Magrini and Roberto D'Amico (RDA) provided input for writing the protocol and review. All authors provided comments on earlier drafts, revised and approved the initial version of the review. SDM, CG and RDA assessed the new studies for inclusion and performed the data extraction. SDM drafted the changes to the text. All authors provided comments, revised and approved the updated version of the review.

 

Declarations of interest

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms

None known.

 

Sources of support

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms
 

Internal sources

  • SaPeRiDoc, Direzione generale sanità e politiche sociali, Regione Emilia-Romagna, Bologna, Italy.

 

External sources

  • No sources of support supplied

 

Differences between protocol and review

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Appendices
  11. What's new
  12. History
  13. Contributions of authors
  14. Declarations of interest
  15. Sources of support
  16. Differences between protocol and review
  17. Index terms

The methods have been updated to reflect the latest Cochrane Handbook for Systematic Reviews of Interventions (Higgins 2011).

* Indicates the major publication for the study

References

References to studies included in this review

  1. Top of page
  2. Abstract
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Characteristics of studies
  19. References to studies included in this review
  20. References to studies excluded from this review
  21. Additional references
  22. References to other published versions of this review
Carter 1989 {published data only}
  • Carter AO, Gelmon SB, Wells GA, Toepell AP. The effectiveness of a prenatal education programme for the prevention of congenital toxoplasmosis. Epidemiology and Infection 1989;103:539-45.
Wallon 2006 {published data only}
  • Gollub EL, Leroy V, Gilbert R, Chêne G, Wallon M, the European Toxoprevention Study Group (EUROTOXO). Effectiveness of health education on Toxoplasma-related knowledge, behaviour, and risk of seroconversion in pregnancy. European Journal of Obstetric & Gynecology and Reproductive Biology 2008;136:137-45.
  • Nguyen DT. Evolution des connaissances et des comportements au cours d'un programme d'éducation prénatal pour la prévention primaire de la toxoplasmose congénitale chez les femmes enceintes séronégatif pour la toxoplasmose. Règion de Lyon, 1994-1995 [Impact on knowledge and behaviour of a prenatal education programme to prevent congenital toxoplasmosis among seronegative pregnant women. Lyon region, 1994-1995] [Masters thesis]. Bordeaux: University of Bordeaux, Juillet 2004.
  • Wallon M, Nguyen Hoang Hanh DT, Peyron F, Chene G. Impact of health education for the primary prevention of toxoplasma infection in pregnancy: lessons from the ERIS study. 16th European Congress of Clinical Microbiology and Infectious Diseases (ECCMID); 2006 April 1-4; Nice, France. 2006:Abstract no: P876.

References to studies excluded from this review

  1. Top of page
  2. Abstract
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Characteristics of studies
  19. References to studies included in this review
  20. References to studies excluded from this review
  21. Additional references
  22. References to other published versions of this review
Breugelmans 2004 {published data only}
Molé 1992 {published data only}
  • Molé JR, Suárez D, Alonso F, Piquera G. This is what we did to prevent congenital toxoplasmosis in Manzanillo [Lo que hacemos para prevenir la toxoplasmosis congénita en Manzanillo]. Revista Cubana de Medicina General Integral 1992;8(4):330-2.
Pawlowski 2001 {published data only}
  • Pawlowski ZS, Gromadecka-Sutkiewicz M, Skommer J, Paul M, Rokossowski H, Suchocka E, et al. Impact of health education on knowledge and prevention behavior for congenital tooplasmosis: the experience in Poznan, Poland. Health Education Research 2001;16(4):493-502.

Additional references

  1. Top of page
  2. Abstract
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Characteristics of studies
  19. References to studies included in this review
  20. References to studies excluded from this review
  21. Additional references
  22. References to other published versions of this review
Alfirevic 2003
Allain 1998
  • Allain JP, Palmer CR, Pearson G. Epidemiological study of latent and recent infection by toxoplasma gondii in pregnant women from a regional population in the UK. Journal of Infection 1998;36:189-96.
Bader 1997
Boyer 2005
  • Boyer KM, Holfels E, Roizen N, Swisher C, Mack D, Remington J, et al. Risk factors for toxoplasma gondii infection in mothers of infants with congenital toxoplasmosis: implications for prenatal management and screening. American Journal of Obstetrics and Gynecology 2005;192:564-71.
Campbell 2004
Chabbert 2004
  • Chabbert E, Lachaud L, Crobu L, Bastien P. Comparison of two widely used PCR primer systems for detection of toxoplasma in amniotic fluid, blood, and tissues. Clinical Microbiology 2004;42:1719-22.
Cook 2000
  • Cook AJ, Gilbert RE, Buffolano W, Zufferey J, Petersen E, Jenum PA, et al. Sources of toxoplasma infection in pregnant women: European multicentre case-control study. European Research Network on Congenital Toxoplasmosis. BMJ 2000;321:142-7.
Dunn 1999
Egger 1997
  • Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997;315(7109):629-34.
EpiInfo 6
  • Dean AG, Dean JA, Coulombier D, Brendel KA, Smith DC, Burton AH, et al. EpiInfo, Version 6: a word processing, database, and statistics programs for epidemiology on microcomputers. Atlanta: Centers for Disease Control and Prevention, 1994.
Ferguson 2011
  • Ferguson W, Mayne PD, Cafferkey M, Butler K. Lack of awareness of risk factors for primary toxoplasmosis in pregnancy. Irish Journal of Medical Science 2011;180:807-11.
Foulon 1988
  • Foulon W, Naessens A, Lauwers S, De Meuter F, Amy JJ. Impact of primary prevention on the incidence of toxoplasmosis during pregnancy. Obstetrics & Gynecology 1988;72:363-6.
Foulon 1994
Foulon 1999a
  • Foulon W, Villena I, Stray-Pederson B, Decoster A, Lappalainen M, Pinon JM, et al. Treatment of toxoplasmosis during pregnancy: a multicenter study of impact on fetal transmission and children sequelae at age 1 year. American Journal of Obstetrics and Gynecology 1999;180:410-5.
Foulon 1999b
  • Foulon W, Pinon JM, Stray-Pederson B, Pollak A, Lappalainen M, Decoster A, et al. Prenatal diagnosis of congenital toxoplasmosis: a multicenter evaluation of different diagnostic parameters. American Journal of Obstetrics and Gynecology 1999;181:843-7.
Gilbert 1999
  • Gilbert RE. Epidemiology of infection in pregnant women. In: Petersen E, Amboise-Thomas P editor(s). Congenital Toxoplasmosis: Scientific Background, Clinical Management and Control. Paris: Springer-Verlag France, 1999.
Gilbert 2001
  • Gilbert R, Dunn D, Wallon M, Hayde M, Prusa A, Lebech M, et al. Ecological comparison of the risks of mother-to-child transmission and clinical manifestations of congenital toxoplasmosis according to prenatal treatment protocol. Epidemiology and Infection 2001;127:113-20.
Gilbert 2002
Gilbert 2003
  • Gilbert R, Gras L. European multicentre study on congenital toxoplasmosis. Effect of timing and type of treatment on the risk of mother to child transmission of Toxoplasma gondii. BJOG: an international journal of obstetrics and gynaecology 2003;110:112-20.
Gilbert 2007
  • Gilbert RE, Thalib L, Tan HK, Paul M, Wallon M, Petersen E. Screening for congenital toxoplasmosis: accuracy of immunoglobulin M and immunoglobulin A tests after birth. Journal of Medical Screening 2007;14:8-13.
Hahn 2005
  • Hahn S, Puffer S, Torgerson DJ, Watson J. Methodological bias in cluster randomised trials. BMC Medical Research Methodology  2005;5:10.
Harbord 2006
Higgins 2011
  • Higgins JPT, Green S, editors. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 [updated March 2011]. The Cochrane Collaboration, 2011. Available from www.cochrane-handbook.org.
Lebech 1996
  • Lebech M, Joynson DH, Seitz HM, Thulliez P, Gilbert RE, Dutton GN, et al. Classification system and case definitions of toxoplasma gondii infection in immunocompetent pregnant women and their congenitally infected offspring. European Research Network on Congenital Toxoplasmosis. European Journal of Clinical Microbiology and Infectious Diseases 1996;15:799-805.
Lebech 1999
  • Lebech M, Andersen O, Christensen NC, Hertel J, Nielsen HE, Petersen B, et al. Feasibility of neonatal screening for toxoplasma infection in the absence of prenatal treatment. Danish Congenital Toxoplasmosis Study Group. Lancet 1999;353:1834-7.
Liesenfeld 1997
  • Liesenfeld O, Press C, Montoya JG, Gill R, Isaac-Renton JL, Hedman K, et al. False-positive results in immunoglobulin M (IgM) toxoplasma antibody tests and importance of confirmatory testing: the Platelia toxo IgM test. Journal of Clinical Microbiology 1997;35:174-8.
Montoya 2004
NSC 2001
  • National Screening Committee Working Group. Antenatal and Newborn Screening for Toxoplasmosis. Report of the Working Group -- October 2001. National Screening Committee, 2001.
Peyron 1999
  • Peyron F, Wallon M, Liou C, Garner P. Treatments for toxoplasmosis in pregnancy. Cochrane Database of Systematic Reviews 1999, Issue 3. [DOI: 10.1002/14651858.CD001684]
Puffer 2003
Reis 1999
  • Reis R, Lösch R, Lago EG. Primary prevention of congenital toxoplsmosis [Prevenção primária da toxoplasmose congênita]. Acta Médica 1999;20:704-20.
RevMan 2011
  • The Nordic Cochrane Centre, The Cochrane Collaboration. Review Manager (RevMan). 5.1. Copenhagen: The Nordic Cochrane Centre, The Cochrane Collaboration, 2011.
Rorman 2006
Schmidt 2006
  • Schmidt DR, Hogh B, Andersen O, Fuchs J, Fledelius H, Petersen E. The national neonatal screening programme for congenital toxoplasmosis in Denmark: results from the initial four years, 1999-2002. Archives of Disease in Childhood 2006;91:661-5.
Signorell 2006
  • Signorell LM, Seitz D, Merkel S, Berger R, Rudin C. Cord blood screening for congenital toxoplasmosis in northwestern Switzerland, 1982-1999. Pediatric Infectious Disease Journal 2006;25:123-8.
SYROCOT 2007
  • Thiébaut R, Leproust S, Chêne G, Gilbert R. Effectiveness of prenatal treatment for congenital toxoplasmosis: a meta-analysis of individual patients' data. Lancet 2007;369:115-22.
Thalib 2005
Torgerson 2001
Wilson 1980
  • Wilson CB, Remington JS, Stagno S, Reynolds DW. Development of adverse sequelae in children born with subclinical congenital Toxoplasma infection. Pediatrics 1980;66:767-74.

References to other published versions of this review

  1. Top of page
  2. Abstract
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Characteristics of studies
  19. References to studies included in this review
  20. References to studies excluded from this review
  21. Additional references
  22. References to other published versions of this review
Di Mario 2006
  • Di Mario S, Basevi V, Gagliotti C, Spettoli D, Gori G, D'Amico R, et al. Prenatal education for congenital toxoplasmosis. Cochrane Database of Systematic Reviews 2006, Issue 4. [DOI: 10.1002/14651858.CD006171]
Di Mario 2009