Seroprevalence of toxoplasmosis in pregnant women

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1 /03/79-01/69 Jornal de Pediatria Copyright 2003 by Sociedade Brasileira de Pediatria Jornal de Pediatria - Vol. 79, Nº1, ORIGINAL ARTICLE Seroprevalence of toxoplasmosis in pregnant women Ivana S. Varella, 1 Mário B.Wagner, 2 Alessandra C. Darela, 3 Leandro M. Nunes, 4 Regina W. Müller 5 Abstract Objectives:: to measure the prevalence of seropositivity for toxoplasmosis in pregnant women and evaluate its association with maternity age, skin color, place of residence and education. Methods: a cross-sectional study in 1,261 pregnant women cared for at the maternity ward of Hospital Nossa Senhora da Conceição was performed from June to October and in December Serological tests for toxoplasmosis were performed during their pregnancy or delivery. The variables considered were place of residence, skin color, education and serum tests for toxoplasmosis (IgG and IgM). Microparticle Enzyme Immunoassay method (MEIA) was used. Results: the prevalence of seropositivity for toxoplasmosis in the pregnant women studied was of 59.8% (95% CI: 57.0% %). An increase in seropositivity in relation to the mother s age was observed (p = 0.012). On the other hand, a higher educational level was found to be a protective factor against toxoplasmosis (p < 0.001). The hypothesis that the proportion of pregnant seropositive women would increase the farther they lived from capital cities was not confirmed (p = 0.750). Differences regarding race were not observed (p = 0.228). In the multivariate analysis, maternity age presented a linear association with the increase of seropositivity, even after adjustment for education, place of residence and skin color. Conclusions: the prevalence of seropositivity in the pregnant women studied is high and justifies the adoption of some primary and secondary preventive measures, until subsequent studies provide greater evidence concerning the rationalization of the diagnostic and therapeutic techniques regarding toxoplasmosis in pregnant women. J Pediatr (Rio J) 2003;79(1):69-74: toxoplasmosis, pregnancy, antibodies, prevalence. Introduction Toxoplasma gondii may be transmitted through the placenta and cause fetal infection when the mother acquires the infection during pregnancy or, less commonly, when chronically infected women are immunocompromised. 1,2 1. Pediatrician and neonatologist. Master s Degree, Universidade Federal do Rio Grande do Sul. 2. Doutor em Epidemiologia. Professor Adjunto, Departamento de Medicina Social - Faculdade de Medicina, UFRGS. 3. Resident physician, Pediatric Program, Hospital da Criança Conceição, Porto Alegre, Rio Grande do Sul. 4. Resident physician, Pediatric Program, Hospital da Criança Conceição, Porto Alegre, Rio Grande do Sul. 5. Pediatrician and neonatologist, Hospital da Criança Conceição, Porto Alegre, Rio Grande do Sul. Manuscript received Mar Accepted for publication Oct Several studies have determined that the main risk factor for infection in pregnant women is the consumption of inadequately cooked meat, which contributed to 30% to 63% of the cases; other infections (6% to 17%) were attributed to contaminated soil. 3,4 Between 1992 and 1994, Kapperud et al. observed in Norway that the subjects had daily contact with cats more frequently than the ones in the control group (OR = 3.6) and that the ones who washed the kitchen knife less frequently had an infection risk five times as high. 5 Another study by these authors showed that the prevalence of IgG antibodies in pregnant women increased significantly in women above 34 years of age. 6 Although the majority of infected neonates do not present any symptoms, almost all of them developed sequelae 69

2 70 Jornal de Pediatria - Vol. 79, Nº1, 2003 Seroprevalence of toxoplasmosis in pregnant women - Varella IS et alii after birth, including chorioretinitis, mental retardation and moderate hearing loss. 7-9 A bilateral macular scar resulting from congenital toxoplasmosis was the greatest cause of reduced visual acuity (43%) in a retrospective study conducted in a clinic of low visual acuity among patients younger than 14 years at Universidade Estadual de Campinas in São Paulo, from 1982 to The prevalence of seropositivity in pregnant women varies according to geographic regions, climatic characteristics, cultural factors and eating habits. 5 A rate of 10.9% was observed in Norway,6 14% in Stockholm, % in London, % in Finland, 13 and 32% in New York City. 1 In Paris, 70% of pregnant women showed seropositivity, but after primary prevention measures, it was reduced to 65%. 1 The recommendations for serological screening differ from country to country because the cost-effectiveness ratio of each program varies according to the prevalence of toxoplasma infection during pregnancy. 7,14,15 In 1978 and 1985, Austria and France implemented national programs for the immediate detection and treatment of toxoplasma infections during pregnancy. The recommendations are that nonimmune pregnant women be tested monthly or once every three months in order to detect seroconversion. 16,17 However, in systematic reviews to evaluate the evidence of the treatment effectiveness during pregnancy, Wallon et al. concluded that the value of the antenatal screening programs depends on the safety of the treatment in reducing the risk of the congenital disease and on the fact that the available data are not comparable to measure the risks and benefits of the antiparasitic drugs used for presumable antenatal toxoplasma infection. 16,18 Since the costs associated with available diagnostic methods and treatments are high, a more reasonable alternative should be primary prevention by identifying the risk factors for toxoplasmosis during pregnancy and providing written guidance to seronegative pregnant women in the first prenatal appointment with their doctor. 5,19,20 A greater prevalence of seropositivity is an indicator of a greater exposure of the population to the determining factors of the disease. In Brazil there are a few studies about the prevalence of seropositive pregnant women for IgG toxoplasma antibodies: 77.1% in Rio de Janeiro, % in Recife, % in Porto Alegre, 23 42% in Salvador, 24 and 32.4% in the metropolitan area of São Paulo. 25 However, considering the eating habits of the population in Rio Grande do Sul and the fact that in rural areas there is a predominance of a lifestyle based on family subsistence agriculture, a high prevalence of seropositivity for toxoplasma infections is expected. The main purpose of this study is to determine the prevalence of seropositivity for toxoplasmosis in pregnant women and verify possible associations between seropositivity and the following factors: age, complexion, educational level and place of origin of mothers. Material and Methods The maternity ward of Hospital Nossa Senhora da Conceição (HNSC) provides tertiary care to the population residing in Porto Alegre and in the Metropolitan Region, and it is a reference center for high-risk pregnancy. An average of 7,000 births a year is observed. Out of a total of 2,610 pregnant women who received labor assistance between July and October and also in December of 2000, 1,261 patients were included in the study. These patients had undergone a serological examination for toxoplasmosis at the central laboratory of this hospital during prenatal exams or at the moment of admission to the maternity ward. The other patients were excluded from the study because they had undergone a serological examination outside the laboratory of the HNSC. This criterion was adopted in order to avoid misclassification bias because the available serological methods present great variability as far as sensitivity and specificity are concerned. 26 The information contained in the medical charts of pregnant women and their newborn babies was collected by means of a data collection form. The medical charts of the month of November were not available due to administrative problems. The serologic method used was the Microparticle Enzyme Immunoassay (MEIA) Abbott Diagnostics AxSYM SYSTEM Toxo IgG and IgM. IgG was considered to be reactive (IgGR) when the concentration was higher than 3 IU/ml and non-reactive (IgGNR) when the quantitation of these antibodies was lower than 2 IU/ml. The amount of IgM was considered reactive (IgMR) when the level was higher than 0.600, and non-reactive when it was lower than The intermediate values, between 2 and 3 IU/ml for IgG concentration and between and for IgM levels were considered doubtful (Manufacturer s manual Abbott AxSYM SYSTEM Toxo IgG. August, 1999). The pregnant women were considered seropositive for toxoplasmosis whether they presented a reactive IgG followed by reactive IgM or not. When the patients presented non-reactive results for IgG and IgM (IgGNR and IgMNR) antibodies, they were considered susceptible to infection. In this cross-sectional study, when the pregnant women showed a serologic result with presence of IgG and IgM antibodies, it was not possible to determine the occurrence of acute infection during pregnancy. In the protocol we used the presence of IgM antibodies and the IgG avidity test and, preferably, the maternal seroconversion documentation to initiate the investigation of newborns concerning the possibility of congenital infection. Immediately after birth, this investigation includes serology for toxoplasmosis (IgG and IgM) and polymerase chain reaction in a serum sample, a complete exam of the cerebrospinal fluid, hemogram, transfontanellar ultrasonography and ophthalmologic evaluation. The empirical treatment is started and the clinical follow-up is

3 Seroprevalence of toxoplasmosis in pregnant women - Varella IS et alii Jornal de Pediatria - Vol. 79, Nº1, maintained through serological tests for toxoplasmosis when the child is one, two, four, six months old or even older, if necessary. The treatment is maintained or interrupted according to the exams and symptomatology of the newborn. Initially, a 25% seroprevalence for toxoplasmosis was estimated for this population. Sample size was calculated for each of the variables studied through the Epi Info 6.04 program, and a larger sample was obtained with 984 pregnant women. Starting from this calculation an approximate value of 20% was added, since analytical approaches that adjust the confusion variables require an increase in the sample size and, with that, a total sample of 1,200 pregnant women was finally obtained. The analysis was based on the binomial distribution through the calculation of a simple ratio to estimate the prevalence of seropositivity for toxoplasmosis and its 95% confidence interval. Several groups were compared and odds ratio (OR), 95% confidence intervals and significance determined by the Chi-square test were obtained. A logistic regression model was elaborated to simultaneously study the multiple effects that may be involved in the prevalence of seropositivity for toxoplasmosis in pregnant women. The data were analyzed by using the SPSS 10.0 (Statistical Package for the Social Sciences) computer program. After a term of commitment was signed by the researches for the utilization of data collected from medical charts referring to patients assisted at the HNSC maternity ward, the research project was evaluated and approved by the Ethics Committee of HNSC and Hospital de Clínicas in Porto Alegre. Results Most of the pregnant women included in the study had had prenatal care in health centers (38.5%) and at the Hospital Nossa Senhora da Conceição (26.6%). Only 7.6% of them had not seen a doctor. In 60.3% of the pregnant women, the serological exam for toxoplasmosis was requested during prenatal care; the data on the remaining patients were collected at the time of birth. The prevalence of seropositivity for toxoplasmosis in the analyzed pregnant women was 59.8% (95% CI: 57.0% %). This result is described in Table 1, as well as the ratio of pregnant women susceptible to infection in pregnancy (IgG NR and IgM NR). Table 1 - Description of the results in 1,261 pregnant women Result f Prevalence 95%CI Seropositivity [IgG (+); IgM ( )] % 54.7% 60.1% [IgG (+); IgM (+)] % 1.6% 3.3% Susceptibility [IgG ( ); IgM ( )] % 37.5% 42.9% The age of seropositive women varied between 13 and 45 years (average±sd = 26.3±7.34). The distribution concerning complexion, educational level and place of origin is described in Table 2. In addition, the results of the bivariate analysis can also be observed in this table. There is a linear trend towards the increase of seropositivity with the increased age of pregnant women (p = 0.012). A higher maternal educational level was identified as a protective factor against toxoplasmosis (p < 0.001). The hypothesis that the number of seropositive pregnant women would increase the higher the distance from the capital city was not confirmed (p = 0.750). The relationship between place of origin and seropositivity showed that the pregnant women residing in Porto Alegre have 1.4 times the risk to be previously infected by Toxoplasma gondii when compared to pregnant women residing in the Metropolitan Region. Besides, there was no difference in the outcome as to complexion (p = 0.228). The multivariate analysis confirmed the previous findings; after an adjustment to match the effects of other terms included in the model, the seropositivity for toxoplasmosis maintained a linear association with age and higher educational level was a protective factor (Table 3). Discussion This study was performed with pregnant women assisted at a public maternity ward located in the northern zone of the city of Porto Alegre. Although prevalence studies increase their validity when they are population-based, there was no loss in our study as to selection bias, even though it was carried out in a restricted population; when the purpose is to establish preventive measures in toxoplasmosis, the target population is that of pregnant women. In addition, toxoplasmosis in adults does not require treatment, except in cases of active chorioretinitis. Another important aspect that was cautiously followed to preserve the internal validity of the study was the selection of pregnant women that had been submitted to serological tests with the same diagnostic method in a single laboratory, preventing therefore misclassification biases. The evaluation of antibody response may have diverse results when different tests are used, but also when the same test is used in other laboratories, since antigen preparations may vary. 1 Furthermore, different laboratory methods present variability as to their sensitivity and specificity. 26 Ideally, the frequency of events must be provided by well-conducted population-based studies, so that all the existing subgroups in the community are properly represented. 27 Although a great portion of the population of pregnant women had already undergone a serological test in other laboratories, and were therefore excluded (53.6%), the authors did not consider the presence of selection bias because the characteristics of the patients do not vary according to this established criterion. In other words, the pregnant women that formed the population under study do

4 72 Jornal de Pediatria - Vol. 79, Nº1, 2003 Seroprevalence of toxoplasmosis in pregnant women - Varella IS et alii Table 2 - Seropositivity for toxoplasmosis in pregnant women according to age, color, educational level and place of origin Variable n f Prev (%) OR 95%CI p Age (years) (a) ( ) ( ) ( ) Color White (a) Mixed ( ) Black ( ) Education (years) 0 to 4 (a) to ( ) to ( ) and more ( ) <0.000 Place of origin Porto Alegre * Metropolitan region ( ) Other cities ( ) * Reference category Table 3 - Seropositivity in pregnant women according to age, color, educational level and place of origin, with effects adjusted in a multivariate logistic regression model Variable OR 90%CI p Mother s age (years) * Color White * 1.00 Mixed Black Education (years) 0 to 4 * to to and more < Place of origin Porto Alegre * 1.00 Metropolitan region Other cities * Reference category not differ from those that were excluded because they have the same socioeconomic profile. The pregnant women studied represent the population that seeks the Unified Health System for basic hospital procedures, even if the complementary examinations are carried out in other public laboratories. However, the studied population does not represent the population of pregnant women of the entire city of Porto Alegre and of the metropolitan region. The confounding bias was controlled by means of the simultaneous analysis of several variables. 28 The studies that measure the occurrence of diseases and that use a more solid framework, such as cohort studies, have the advantage of better defining the agents that cause the risk factors due to the follow-up of the studied population over time. Nevertheless, to determine the prevalence of seropositivity for toxoplasmosis in pregnant women, which is the purpose of this study, such a design would be scarcely feasible because it would increase the costs and the period necessary for its execution. 28 The advantage is that the measurements obtained by a prevalence study, relative risk or odds ratio allow us to estimate the magnitude of an association between the exposure and the disease and to indicate the probability of development of the disease in the group of exposed

5 Seroprevalence of toxoplasmosis in pregnant women - Varella IS et alii Jornal de Pediatria - Vol. 79, Nº1, individuals in relation to the ones that have not been exposed. 29 The serologic method used in this study for the detection of IgG antibodies presents sensitivity and specificity of 98.9% and 98.3%, respectively. 30 The studies carried out to measure the discrepancy between the commercially available tests have found more flaws in the detection of IgM antibodies (10%) than in the detection of IgG antibodies (8%). This limitation to the interpretation of IgM results is increased when these are applied to a population with low prevalence of toxoplasmosis. 30 Thus, the results of this study concerning the number of pregnant women with reactive IgM antibodies are not reliable for the diagnosis of acute infection. For that to happen, it would be necessary to carry out a study with another experimental design that would allow the observation of serial tests, apart from the use of diagnostic methods that provide a better estimate of the period in which the acute infection occurred. The conventional immunoenzyme assays currently available for the demonstration of specific IgM antibodies present high sensitivity and low specificity with a high probability of false positive results. 26,31 Moreover, Naot & Remington demonstrated that these antibodies were not detected after a year or more as from the onset of the clinical symptoms. Therefore, they may persist for several months or even years after an acute infection episode. 32 For the final diagnosis of acute infection in pregnancy, serial tests would be necessary to identify maternal seroconversion when previously diagnosed as susceptible to infection or, yet through the use of confirmatory tests. A recent infection marker is the low affinity or avidity of IgG antibodies. It is a simple test that may complement the definition of a serological profile, especially when insufficiently outlined by the other serological markers. 33,34 Some authors state that the low avidity of IgG should not be interpreted as a recently acquired infection because it may persist for over five months, depending on the technique used. However, the high avidity of IgG in the first trimester of pregnancy virtually excludes recently acquired infection, which makes this test useful at the beginning of pregnancy. But the high avidity at a later phase of pregnancy does not exclude infection acquired in the first trimester. 1 When the prevalence found in this study is compared with data available in the literature, we observe a large number of pregnant women that have already had toxoplasma infection. These results are similar to those found in a study carried out in France in 1995, in which seroprevalence reached 54.3%. In Paris, seroprevalence decreased from more than 80% in 1960 to 72% in In 1995, it remained high (65%).1 This seropositivity rate is within the limits of prevalence found in Brazil, which varied from 32.4% in São Paulo25 to 77.1% in Rio de Janeiro. 21 The educational level of mothers presented a clear protective effect for toxoplasma seropositivity (p < 0.001), especially after nine years in school. This inverse association supports the hypothesis that the level of education decreases risk exposure due to the adoption of more appropriate hygiene measures regarding eating habits. In addition, age showed a slight increase in the risk of seropositivity, which demonstrated statistic significance as from 32 years of age (p = 0.059). This association is explained by the longer time of exposure to the causing agent. Such finding confirms the importance of routine serologic screening in pregnant women. A paradox finding of the study is a slight protective effect observed in women about to give birth residing in the metropolitan region in relation to the ones living in Porto Alegre. As far as the other cities are concerned, there was a slight risk, but no statistical significance was observed (p = 0.173). Among all the studied variables, the one that showed the highest risk was educational level lower than 9 years (OR = 2.2). This demonstrates the importance of investments directed to the access and to the quality of teaching in our population as a way to promote their health. When the variables were introduced in the model of logistic regression for simultaneous analysis, we observed odds ratios that were very similar to the findings of the unadjusted and crude analysis. This shows the independence of the effects observed in the different variables, with no interference from the confounding factor. The study revealed a high prevalence of seropositivity for toxoplasmosis in pregnant women. It is important to emphasize that the risk of exposure increases in the pregnant women who reside in Porto Alegre, in those who have an educational level below seven years and in those who are older than 32 years. If the disease was acquired prior to infection, attention should be focused on susceptible pregnant women (40.2%), who have risk of acute infection and, consequently, fetal transmission. If, on the one hand, the study showed a high prevalence of infection before pregnancy, the remaining susceptible ones are more often exposed to pathological agents. There are still no studies that emphasize the benefits of maternal treatment to prevent vertical transmission; therefore, verbal and written orientation of preventive measures to the susceptible pregnant women who have prenatal care at public health centers or hospitals, as well as the routine screening in this population would allow identifying and decreasing the cases of acute infection in pregnant women. Consequently, this would reduce the amount of cases of congenital infection and the appearance of sequelae in the future through the early implementation of treatment in congenitally infected children. References 1. Remington JS, McLeod R, Thulliez P, Desmonts G. Toxoplasmosis. In: Remington JS, Klein JO, eds. Infectious diseases of the fetus and newborn infant. 5th ed. Philadelphia: WB Saunders; p

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