Seroepidemiology of Toxoplasma Gondii in Pregnant Women in Aguascalientes City, Mexico: a Cross-Sectional Study
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Open Access Research BMJ Open: first published as 10.1136/bmjopen-2016-012409 on 1 July 2016. Downloaded from Seroepidemiology of Toxoplasma gondii in pregnant women in Aguascalientes City, Mexico: a cross-sectional study Cosme Alvarado-Esquivel,1 María del Carmen Terrones-Saldívar,2 Jesús Hernández-Tinoco,3 María Daniela Enriqueta Muñoz-Terrones,2 Roberto Oswaldo Gallegos-González,2 Luis Francisco Sánchez-Anguiano,3 Martha Elena Reyes-Robles,2 Fernando Jaramillo-Juárez,2 Oliver Liesenfeld,4,5 Sergio Estrada-Martínez3 To cite: Alvarado-Esquivel C, ABSTRACT Strengths and limitations of this study Terrones-Saldívar M del C, Objectives: We determined the seroprevalence and Hernández-Tinoco J, et al. correlates of Toxoplasma gondii infection in pregnant ▪ Seroepidemiology of This is the first cross-sectional study of women in Aguascalientes City, Mexico. Toxoplasma gondii in Toxoplasma gondii infection in pregnant women pregnant women in Design: A cross-sectional survey. in the central Mexican city of Aguascalientes. Aguascalientes City, Mexico: Setting: Pregnant women were enrolled in the central ▪ The current study gave us the immunological a cross-sectional study. BMJ Mexican city of Aguascalientes. status against infection with T. gondii in a Open 2016;6:e012409. Participants: We studied 338 pregnant women who sample of pregnant women in central Mexico. doi:10.1136/bmjopen-2016- attended prenatal care in 3 public health centres. ▪ This study provides a number of risk factors for 012409 Primary and secondary outcome measures: infection with T. gondii in pregnant women that Women were examined for IgG/IgM antibodies to can be useful to design optimal preventive mea- ▸ Prepublication history for T. gondii by using commercially available enzyme sures against toxoplasmosis. this paper is available online. immunoassays, and an avidity test. Multiple analyses ▪ The sample size was small, and the seropositivity To view these files please were used to determine the association of T. gondii rate was low to perform a wider analysis of the visit the journal online seropositivity with the characteristics of the pregnant association of T. gondii exposure and character- (http://dx.doi.org/10.1136/ istics of the pregnant women. http://bmjopen.bmj.com/ bmjopen-2016-012409). women. Results: Of the 338 pregnant women studied, 21 Received 24 April 2016 (6.2%) had IgG antibodies to T. gondii, and 1 (4.8%) with oocysts shed by cats or other felids, by Revised 26 May 2016 of them was also positive for IgM antibodies to ingestion of tissue cysts in meat from mammals Accepted 7 June 2016 T. gondii. Avidity of IgG antibodies to T. gondii was and birds,23and congenitally.45Most infec- high in the IgM-positive sample. Logistic regression tions are asymptomatic; however, infection with analysis of sociodemographic, behavioural and housing variables showed that T. gondii seropositivity was the parasite can lead to acute toxoplasmosis associated with white ethnicity (OR=149.4; 95% CI that presents as lymphadenopathy or choriore- 5 10.8 to 2054.1; p<0.01), not washing hands before tinitis. Immunocompromised individuals may on September 28, 2021 by guest. Protected copyright. eating (OR=6.41; 95% CI 1.73 to 23.6; p=0.005) and develop a life-threatening disease with menin- use of latrine (OR=37.6; 95% CI 4.63 to 306.31; goencephalitis.56Primary infection with p=0.001). T. g o n d i i during pregnancy may lead to con- Conclusions: Results demonstrate that pregnant genital disease with miscarriages or still- women in Aguascalientes City have a low births,578or disease in eye and central nervous seroprevalence of T. gondii infection. However, this low system.5910Most newborns with congenitally prevalence indicates that most pregnant women are at acquired infections with T. g o n d i i are asymptom- risk for a primary infection. Factors associated with atic; however, clinical manifestations of toxo- T. gondii exposure found in this study, including food plasmosis develop later in life.9 Diagnosis of hygiene, may be useful to determine preventive measures against T. gondii infection and its sequelae. infection with T. gondii during pregnancy is made with the aid of serological tests, particu- larly the IgG avidity testing that allows for more 11 12 For numbered affiliations see accurate timing of maternal infection. end of article. INTRODUCTION Very little is known about the seroepide- Infection with the parasite Toxoplasma gondii miology of T. gondii infection in pregnant Correspondence to (T. gondii) is common in humans and animals women in Mexico in general, and there is a 12 Dr Cosme Alvarado-Esquivel; around the world. This infection is acquired lack of knowledge about this infection in [email protected] by ingestion of water or food contaminated pregnant women, particularly in the central Alvarado-Esquivel C, et al. BMJ Open 2016;6:e012409. doi:10.1136/bmjopen-2016-012409 1 Open Access BMJ Open: first published as 10.1136/bmjopen-2016-012409 on 1 July 2016. Downloaded from Mexican city of Aguascalientes. In two previous studies in were obtained with the aid of a standardised question- the northern Mexican state of Durango, T. g o n d i i seropre- naire. Sociodemographic items included age, ethnic valences of 6.1% in urban13 and 8.2% in rural14 pregnant group, birthplace, residence place, residence area, edu- women were found. In the present study, we sought to cational level, occupation and socioeconomic status. determine the seroprevalence of T. g o n d i i infection in Clinical data included health status; presence or history pregnant women attending prenatal consultations at three of lymphadenopathy; presence of frequent abdominal public health centres in Aguascalientes City, Mexico, and pain or headaches; impairments of memory, reflexes, to determine the association of T. g o n d i i seropositivity with vision and hearing; history of surgery; hepatitis; blood the sociodemographic, clinical, behavioural and housing transfusions or transplants; and obstetric history characteristics of the pregnant women. (number of pregnancies, deliveries, caesarean sections, miscarriages and stillbirths). Behavioural items included presence of cats at home, cats in the neighbourhood, MATERIALS AND METHODS raising farm animals, foreign travel, consumption of raw Study design and study population or undercooked meat, type of meat consumed (pork, Through a cross-sectional study design, we examined lamb, beef, goat, boar, chicken, turkey, rabbit, deer, pregnant women who attended the prenatal care consulta- squirrel, horse, etc), eating away from home (in restau- tions at one of the three public health centres (Instituto rants and fast food outlets), consumption of dried or de Servicios de Salud del Estado de Aguascalientes) in cured meat (chorizo, ham, sausages or salami) or Aguascalientes City, Mexico, from October 2014 to animal brains, unwashed raw vegetables or fruits, February 2016. Aguascalientes is located in central Mexico; untreated water or unpasteurised milk, soil contact (gar- its coordinates and climate conditions are shown in dening or agriculture), and washing hands before fi gure 1. Inclusion criteria were: (1) pregnant women with eating. Housing conditions included type of flooring, – – 1 9 months of pregnancy; (2) aged 13 45 years and (3) form of elimination of excretes and crowding. who accepted to participate in the study. Socioeconomic status, occupation, or educational level were not restrictive Detection of anti-T. gondii antibodies criteria for enrolment. Participants were enrolled consecu- A serum sample was obtained from each pregnant tively. In total, 338 pregnant women (mean age 22.95 women. Sera were stored at −20°C until analysed. All – ±6.19 years; range 13 42 years) were included in the study. serum samples were tested for IgG antibodies to T. gondii by a commercially available enzyme immunoassay Sociodemographic, clinical, behavioural and housing ‘Toxoplasma IgG’ kit (Diagnostic Automation/Cortez characteristics of the pregnant women Diagnostics, Woodland Hills, California, USA). Sera posi- Sociodemographic, clinical and behavioural character- tive for IgG antibodies to T. gondii were further tested http://bmjopen.bmj.com/ istics, and housing conditions of the pregnant women for IgM antibodies to T. gondii by a commercially on September 28, 2021 by guest. Protected copyright. Figure 1 Geographical location of Aguascalientes State, Mexico. It is located in central Mexico, and the geographical coordinates of its capital (Aguascalientes City) are 21°53′N, 102°18′W. This city has a temperate semiarid climate, a mean annual rainfall of 500 mm, an altitude of 1700 m above sea level and a mean annual temperature of 18.5°C. 2 Alvarado-Esquivel C, et al. BMJ Open 2016;6:e012409. doi:10.1136/bmjopen-2016-012409 Open Access BMJ Open: first published as 10.1136/bmjopen-2016-012409 on 1 July 2016. Downloaded from available enzyme immunoassay ‘Toxoplasma IgM’ kit Table 1 Sociodemographic characteristics of pregnant (Diagnostic Automation/Cortez Diagnostics). Positive women and prevalence of Toxoplasma gondii infection samples for IgM antibodies to T. g o ndi i by enzyme immunoassay were further tested with the commercially Prevalence of T. gondii available enzyme-linked fluorescence immunoassay infection (ELFA) kit ‘VIDAS Toxo IgM’ (bioMérieux, Marcy Characteristic N N Per cent p Value l’Etoile, France). Seropositivity for IgM antibodies was considered when both (enzyme immunoassay (EIA) and Age groups (years) ELFA) IgM tests were positive. Avidity of IgG antibodies to 20 or less 141 10 7.1 0.54 – T. g o n d i i was assessed in IgM seropositive samples by the 21 30 151 10 6.6 31 or more 41 1 2.4 VIDAS TOXO IgG Avidity (bioMérieux) assay. All tests ’ Ethnic group were performed following the manufacturer sinstruc- Mestizo 312 17 5.4 0.001 tions. Positive and negative controls were included in White 4 3 75.0 each run. Birth place Aguascalientes State 284 18 6.3 0.96 Statistical analysis Other Mexican State 51 3 5.9 Statistical analysis was performed with the aid of Epi Info Abroad 1 0 0.0 V.7 and SPSS V.15.0 software.