Seroepidemiology of Toxoplasma Gondii Infection in Pregnant Women in Rural Durango, Mexico

J. Parasitol., 95(2), 2009, pp. 271–274 ᭧ American Society of Parasitologists 2009 SEROEPIDEMIOLOGY OF TOXOPLASMA GONDII INFECTION IN PREGNANT WOMEN IN RURAL DURANGO, MEXICO C. Alvarado-Esquivel, A. Torres-Castorena*, O. Liesenfeld†, C. R. Garcıá-Lo´ pez‡, S. Estrada-Martıńez§, A. Sifuentes-A´ lvarez, J. F. Marsal-Hernańdez, R. Esquivel-Cruz࿣, F. Sandoval-Herrera*, J. A. Castan˜ eda*, and J. P. Dubey#¶ Faculty of Medicine, Jua´rez University of Durango State, Avenida Universidad S/N esquina Fanny Anitua, 34000 Durango, Dgo, Mexico. e-mail: [email protected] ABSTRACT: The epidemiology of Toxoplasma gondii infection in pregnant women in rural Mexico is largely unknown. The seroepidemiology of T. gondii infection in 439 pregnant women from 9 communities in rural Durango State, Mexico was investigated. Using commercial enzyme-linked immunoassays, sera were tested for T. gondii IgG, IgM, and avidity antibodies. Prevalences of T. gondii IgG antibodies in the communities varied from 0% to 20%. Overall, 36 (8.2%) of the 439 women had IgG T. gondii antibodies. Ten (2.3%) women had also T. gondii IgM antibodies; IgG avidity was high in all IgM-positive women, suggesting chronic infection. None of the women, however, had delivered a known T. gondii-infected child. The seroprevalence was significantly higher (P Ͻ 0.05) in women from low socio-economic conditions (14%) than in those with higher socio-economic status (6.6%). Multivariate analysis showed that T. gondii infection was associated with soil floors at home (adjusted OR ϭ 2.89; 95% CI: 1.12–7.49). This is the first epidemiological study of T. gondii infection in pregnant women in rural Mexico. Toxoplasma gondii has a worldwide distribution. Most T. women, of all ages and at any stage of pregnancy, residing in rural gondii infections are asymptomatic and, in some individuals, a Durango State. mild disease including cervical lymphadenopathy or ocular Epidemiological data problems may occur (Montoya and Liesenfeld, 2004; Hill et al., Epidemiological data, including socio-demographic, behavioral, and 2005). Primary infection during pregnancy may result in severe clinical characteristics, were obtained from all pregnant women. Socio- damage to the fetus (Montoya and Liesenfeld, 2004; Rorman demographic characteristics included age, birth place, place of residen- et al., 2006). Epidemiological studies on T. gondii infection in cy, occupation, and educational and socio-economic levels. Behavioral pregnant women have focused largely on urban populations. characteristics included animal contacts, removal of cat excrement, for- The epidemiology of T. gondii infection in pregnant women in eign travel, contact with soil (gardening or agriculture), eating outside of the home, consumption of raw or undercooked meat (pork, lamb, rural Mexico is essentially unknown. We recently reported se- beef, goat, boar, chicken, turkey, rabbit, deer, squirrel, horse, fish, snake, roprevalences of 14.8% to 35.8% T. gondii antibodies among or other), consumption of dried or cured meat (chorizo, ham, sausages, inhabitants of 3 rural communities in Durango, Mexico (Alva- or salami), consumption of unpasteurized milk, milk products, or water, rado-Esquivel et al., 2008). In the present study, we report se- and unwashed raw vegetable or fruit consumption. Clinical characteristics encompassed gestational age, number of pregnancies and abor- roprevalence and associated epidemiological characteristics of tions, and blood transfusions or transplants, as well as impairment of T. gondii infection in pregnant women from wider rural areas memory, reflexes, hearing, or visual status. Clinical data were obtained in Durango State, Mexico. during a direct interview with the participants. Serological tests MATERIALS AND METHODS Sera of all pregnant women were assayed for T. gondii antibodies Study population and study design using commercially available enzyme immunoassay kits. IgG antibodies were assayed using a ‘‘Toxoplasma IgG’’ kit (Diagnostic Automation From August 2007 to February 2008 we studied pregnant women of Inc., Calabasas, California). Sera positive for T. gondii IgG antibodies 9 rural communities (5 de mayo, Colonia Hidalgo, Guadalupe Victoria, were further tested for T. gondii IgM antibodies with a ‘‘Toxoplasma Santa Clara, Vicente Guerrero, Canatlań, Nuevo Ideal, Santiago Papas- IgM’’ kit (Diagnostic Automation Inc.) and T. gondii IgG avidity kit quiaro, and Rodeo) in Durango State, Mexico. All pregnant women (VIDAS Toxo IgG Avidity, BioMe´rieux, Marcy L’Etoile, France) to attending public prenatal care clinics in the communities were invited help determine the timing of infection, e.g., low-avidity antibodies are to participate. Inclusion criteria for the study subjects were pregnant often associated with recently acquired infection (Petersen et al., 2005). All 3 tests were performed following the instructions of the manufac- turers. A positive IgG test with a negative IgM test, and a positive IgM Received 21 August 2008; revised 29 September 2008; accepted 6 test with a high IgG avidity, was interpreted as a latent infection. October 2008. * Mexican Social Security Institute, Avenida Normal, Predio Canoas Ethical aspects #200, 34000, Durango City, Durango, Mexico. This study was approved by the ethical committee of the General † Institute for Microbiology and Hygiene, Campus Benjamin Franklin, Hospital of the Mexican Social Security Institute in Durango City, Mex- Charite´ Medical School, Hindenburgdamm 27, D-12203 Berlin, Ger- ico. The purpose and procedures of the study were explained to all many. pregnant women, and written, informed consent was obtained from all ‡ Hospital of Santiago Papasquiaro, Dgo. Domicilio Conocido, Santiago of them. Papasquiaro, Durango, Me´xico. § Institute for Scientific Research, Jua´rez University of Durango State, Statistical analysis Avenida Universidad S/N esquina Fanny Anitua, 34000 Durango City, Durango, Mexico. The statistical analysis was performed using Epi Info version 3.3.2 ࿣ Health Center of Santa Clara, Dgo, Domicilio Conocido, Santa Clara, (CDC, Atlanta, Georgia) and SPSS version 13.0 (SPSS Inc., Chicago, Durango, Me´xico. Illinois). We used the Yates corrected ␹2 and the Fisher’s exact test # United States Department of Agriculture, Agricultural Research Ser- (when values were Ͻ5) for comparison of frequencies among groups. vice, Animal and Natural Resources Institute, Animal Parasitic Dis- Bivariate and multivariate analyses were used to assess the association eases Laboratory, Building 1001, Beltsville, Maryland 20705-2350. between the characteristics of the women and T. gondii seropositivity. ¶ To whom correspondence should be addressed. As a criterion for inclusion of variables in the multivariate analysis, we 271 272 THE JOURNAL OF PARASITOLOGY, VOL. 95, NO. 2, APRIL 2009 TABLE I. Selected general characteristics of pregnant women in rural communities of Durango, Mexico. Communities with low Communities with high seroprevalence (Ͻ8.2%) seroprevalence (Ͼ8.2%) All communities Prevalence of T. gondii Prevalence of T. gondii Prevalence of T. gondii No. of No. of No. of infection infection infection women women women Characteristic tested* No. % tested* No. % tested* No. % Age groups (years) 20 or less 86 3 3.5 47 5 10.6 133 8 6.0 21–30 158 8 5.1 66 12 18.2 224 20 8.9 Ͼ30 51 2 3.9 25 6 24 76 8 10.5 Education No education 5 0 0 4 1 25 9 1 11.1 Education 290 13 4.5 135 22 16.3 425 35 8.2 Occupation Unemployed† 253 13 5.1 127 21 16.5 380 34 8.9§ Employed‡ 39 0 0 10 0 0 49 0 0.0 Socio-economic level Low 40 4 10 60 10 16.7 100 14 14§ Medium 253 9 3.6 81 13 16 334 22 6.6 * Pregnant women for which data were available. † Unemployed ϭ no occupation, student, or housewife. ‡ Employed ϭ employee, professional, business, or other. § Statistically significant difference among the groups, P Ͻ 0.05. considered variables with a P-value Յ0.25 obtained in the bivariate pregnancies at the time they were included in the study. Un- analysis in order to allow interaction among variables. Adjusted odd employed women, students, or housewives had a significantly ratio (OR) and 95% confidence interval (CI) were calculated by mul- Ͻ tivariate analysis using multiple, unconditional logistic regression. A P- higher (P 0.05) seroprevalence (8.9%) than employed women value Ͻ0.05 was considered statistically significant. (0%). Similarly, women from a low socio-economic level had a significantly higher (P Ͻ 0.05) seroprevalence (14%) than RESULTS women from medium socio-economic conditions (6.6%). Se- roprevalence showed a slight, but not significant, increase with Seroprevalence age in communities with high seropositivity and in the whole In total, 439 pregnant women consented to be included in population. No significant differences in age, education, and this project. Of these women, 36 (8.2%) had IgG antibodies occupation were observed in women among low- and high- and 10 (2.3%) also had IgM antibodies; all 10 women with prevalence communities. However, a significantly higher (P Ͻ IgM antibodies also had high (0.587; 0.528; 0.587; 0.715; 0.34; 0.001) number of women with low socio-economic status 0.4; 0.522; 0.373; 0.719; 0.723) IgG avidity, indicating latent (42.6%) were observed in high-prevalence communities than in T. gondii infection. Seroprevalences in individual communities low-prevalence (13.7%) communities. General socio-demo- ranged from 0% to 20%: (1) 5 de mayo 16.7% (3/18); (2) Co- graphic characteristics of the 439 rural pregnant women, and lonia Hidalgo 0% (0/8); (3) Guadalupe Victoria 6.5% (3/46); seroprevalences, are shown in Table I. (4) Santa Clara 20% (1/5); (5) Vicente Guerrero 2% (1/49); (6) Canatlań 5.7% (7/123); (7) Nuevo Ideal 7.7% (1/13); (8) San- tiago Papasquiaro 15.8% (19/120); and (9) Rodeo 1.8% (1/57). Behavioral characteristics associated with seropositivity Based on the mean seroprevalence (8.2%) found in women of In the bivariate analysis, several variables were identified as all communities, and for comparison purposes, we decided to possible risk factors associated with T.

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