• View in gallery

    Geographic localization of Colombia and of Cali, the largest city in the western region.

  • View in gallery

    Seroprevalence by age for the low, middle, and high socioeconomic strata (SES) and statistical trends within each SES: * in the low SES χ22) for linear trend = 9.53 P = 0.002, ** in the middle SES χ2 = 4.28 P = 0.07, *** in the high SES χ2 = 0.14 P = 0.704

  • View in gallery

    Maps of Cali, Colombia: (A) Geographic distribution of pregnant women positive for IgG toxoplasma antibodies; (B) Individual women who had both IgG and IgM toxoplasma antibodies (black dots) shown in relation to social and economically deprived areas (See text).

  • 1

    Remington JS, McLeod R, Thulliez P, Desmonts G, 2006. Toxoplasmosis. Chapter 31. In: JS Remington and J Klein, eds. Infectious Diseases of the Fetus and Newborn Infant (6th ed.). WB Saunders, Philadelphia, 947–1092.

  • 2

    Montoya JG, Liesenfeld O, 2004. Toxoplasmosis. Lancet 363 :1965–1976.

  • 3

    Smith KL, Wilson M, Hightower AW, Kelley PW, Struewing JP, Juranek DD, McAuley J, 1996. Prevalence of Toxoplasma gondii antibodies in US military recruits in 1989: comparison with data published in 1965. Clin Infect Dis 23 :1182–1183.

    • Search Google Scholar
    • Export Citation
  • 4

    Remington JS, Efron B, Cavanaugh E, Simon HJ, Trejos A, 1970. Studies on toxoplasmosis in El Salvador. Prevalence and incidence of toxoplasmosis as measured by the Sabin-Feldman dye test. Trans R Soc Trop Med Hyg 64 :252–267.

    • Search Google Scholar
    • Export Citation
  • 5

    Frenkel JK, 1980. Ruiz. Human Toxoplasmosis and cat contact in Costa Rica. Am J Trop Med Hyg 29 :1167–1180.

  • 6

    Bahia-Oliveira LM, Jones JL, Azevedo-Silva J, Alves CC, Orefice F, Addiss DG, 2003. Highly endemic, waterborne toxoplasmosis in north Rio de Janeiro state, Brazil. Emerg Infect Dis 9 :55–62.

    • Search Google Scholar
    • Export Citation
  • 7

    Neto EC, Anele E, Rubim R, Brites A, Schulte J, Becker D, Tuuminen T, 2000. High prevalence of congenital toxoplasmosis in Brazil estimated in a 3-year prospective neonatal screening study. Int J Epidemiol 29 :941–947.

    • Search Google Scholar
    • Export Citation
  • 8

    Glasner PD, Silveira C, Kruszon-Moran D, Martins MC, Burnier Junior M, Silveira S, Camargo ME, Nussenblatt RE, Kaslow RA, Belfort Junior R, 1992. An unusually high prevalence of ocular toxoplasmosis in southern Brazil. Am J Ophthalmol 114 :136–144.

    • Search Google Scholar
    • Export Citation
  • 9

    Zapata M, Reyes L, Holst I, 2005. Disminución en la prevalencia de anticuerpos contra toxoplasma gondii en adultos del valle central de Costa Rica. Parasitol Latinoam 60 :32–37.

    • Search Google Scholar
    • Export Citation
  • 10

    Gómez Marín JE, Castaño JC, Montoya MT, 1995. Toxoplasmosis congénita en Colombia: un problema subestimado de salud pública. Colomb Med 26 :66–70.

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    • Export Citation
  • 11

    Gomez JE, 1997. A maternal screening program for congenital toxoplasmosis in Quindio, Colombia and application of mathematical models to estimate incidences using age-stratified data. Am J Trop Med Hyg 57 :180–186.

    • Search Google Scholar
    • Export Citation
  • 12

    Juliao O, Corredor A, Moreno GS, Estudio Nacional de Salud: Toxoplasmosis en Colombia, Ministerio de Salud. Bogotá 1988; Imprenta Instituto Nacional de Salud

  • 13

    Ancelle T, Goulet V, Tirard-Fleury V, Baril L, Mazaubrun C, Thulliez Ph, Weislo M, Carme B, 1996. La toxoplasmosis chez la femme enceinte en France en 1995. Bull Epidemiol Hebdom Direct Gen 51 :227–228.

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    Henri T, Jacques S, Rene L, 1992. Twenty-two years screening for toxoplasmosis in pregnancy: Liege, Belgium. Scand J Infect Dis 84 (Suppl):84–85.

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    Ades AE, Nokes DJ, 1993. Modeling age and time specific incidence from seroprevalence: Toxoplasmosis. Am J Epidemiol 137 :1022–1034.

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    Jones JL, Kruszon-Moran D, Wilson M, 2003. Toxoplasma gondii infection in the United States, 1999–2000. Emerg Infect Dis 9 :1371–1374.

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    Gallego-Marin C, Henao AC, Gomez-Marin JE, 2006. Clinical validation of a western blot assay for congenital toxoplasmosis and newborn screening in a hospital in Armenia (Quindio) Colombia. J Trop Pedriatr 52 :107–112.

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    Lopez-Castillo C, 2005. Diaz-Ramirez J, Gomez-Marin J. Risk factors for Toxoplasma gondii infection in pregnant women in Armenia, Colombia. Rev Salud Publica (Bogota) 7 :180–190.

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  • 20

    Jes JT, Rosso F, Montoya JG. Perception of pregnant women towards threat of congenital toxoplasmosis. International Conference on Women and Infectious Diseases: progress in science and action. March 16–18, 2006. Atlanta, GA. Abstract No 89, pages 82–83.

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    Nokes DJ, Forsgren M, Gille E, Ljungstrom I, 1993. Modelling toxoplasma incidence from longitudinal seroprevalence in Stockholm, Sweden. Parasitology 107 :33–40.

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    Diza E, Frantzidou F, Souliou E, Arvanitidou M, Gioula G, Antoniadis A, 2005. Seroprevalence of Toxoplasma gondii in northern Greece during the last 20 years. Clin Microbiol Infect 11 :719–723.

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    Nowakowska D, Stray-Pedersen B, Spiewak E, Sobala W, Matafiej E, 2006. Wilczynski. Prevalence and estimated incidence of Toxoplasma infection among pregnant women in Poland: a decreasing trend in the younger population. Clin Microbiol Infect 12 :913–917.

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Prevalence of Infection with Toxoplasma gondii among Pregnant Women in Cali, Colombia, South America

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  • 1 Division of Infectious Diseases and Geographic Medicine, Stanford University School of Medicine, Stanford, California; Toxoplasma Serology Laboratory, Palo Alto Medical Foundation Research Institute, Palo Alto, California; Fundación Clínica Valle del Lili, Departament of Gynecology/Obstetrics, Universidad del Valle; Hospital Universitario del Valle, Comfenalco—Valle EPS, Hospital Joaquín Paz Borrero, Cali, Colombia, South America

The aim of this study was to determine the prevalence of toxoplasma antibodies among pregnant women in Cali, Colombia. In 2005, 955 pregnant women were tested for IgG and IgM antibodies and sociodemographic information was collected. Their average age was 25.1 years, overall IgG seroprevalence 45.8% (95% CI: 41.8%, 48.2%), IgM 2.8% (95% CI: 1.5%, 3.6%). Seroprevalence increased significantly with age, 39.0% in 14 to 19 years to 55.3% in 30 to 39 years (P = 0.001). There was a significant trend toward a higher seroprevalence in the lower socioeconomic strata (SES) (low: 49.0%, high: 29%, P = 0.004). The increase in seroprevalence by age was more significant in the lower socioeconomic strata (P = 0.002). Our results suggest a higher prevalence when compared with those of the national 1980 (33–37.6%) survey. In contrast to reports from other regions of the world, Cali has not seen a decrease in T. gondii seroprevalence over the past 25 years.

INTRODUCTION

Toxoplasma gondii is a protozoan parasite estimated to infect over one billion people worldwide. Two main routes of transmission have been described in humans—by oral ingestion of the parasite and through placental transmission to the fetus. The organism is horizontally transmitted to humans by accidental ingestion of water, food, or soil contaminated with T. gondii oocysts or consumption of meat containing T. gondii cysts that is eaten raw or undercooked. T. gondii can be vertically transmitted to the fetus during pregnancy and may cause a wide range of clinical manifestations in the offspring depending on the gestational age at which the primary maternal infection was acquired, the virulence of the parasite, and the immunologic development of the fetus.1,2

The prevalence of T. gondii infection in the general population of several countries including France, Belgium, and the United Kingdom and the incidence of congenital toxoplasmosis have been reported to be decreasing over the past few decades.1,2 The United States, with a lower overall seroprevalence than Western Europe, has also witnessed a decreased seroprevalence in the general population.3 Several studies have shown a higher overall seroprevalence (> 60%) in Central America and South America (especially in El Salvador,1,4 Costa Rica,5 and Brazil68). However, most studies from the latter regions have not addressed trends of seroprevalence over the past 3 decades with the exception of a study from Costa Rica that revealed a decrease in seroprevalence in the central valley region of the country.9

Although it has been suggested that toxoplasmosis is a public health problem in Colombia, it has received little or no attention.10,11 In 1980, the Ministry of Public Health and the National Institutes of Health of Colombia performed a national seroprevalence study by using an indirect immunofluorescence antibody test to detect IgG toxoplasma antibodies in a randomly selected sample of 9,139 people widely representing the Colombian population. This national survey determined the overall age-adjusted prevalence at 47%, with an increasing prevalence of the infection with age. Important was the observation of variations among geographical regions. The seroprevalence was higher in the Atlantic coast (63%) and lower in the Pacific region (36%).12 Currently in Cali (the largest city of the Pacific region), local physicians—including infectious diseases specialists, ophthalmologists, obstetricians, pediatricians, and general practitioners—believe that toxoplasmosis appears to be both a common and significant cause of clinical illness. Despite these perceptions, epidemiologic or clinical studies have not been performed in Cali or adjacent areas to determine whether toxoplasmosis is a cause of significant illness in high-risk individuals, including immunocompromised patients or those with ocular disease and whether it is a significant cause of infection during gestation thereby placing the fetus and newborn at risk.

The purpose of this study was to perform a seroprevalence survey in pregnant women in Cali, Colombia as a first step toward a better understanding of the adverse impact that toxoplasmosis may be having on its people.

MATERIALS AND METHODS

Study area.

The city of Cali, located in the Southwest region of Colombia (approximately 3°27′N latitude and 76°32′W longitude; at an altitude of 995 m above the sea level, with an area of 542 km2) has a population of approximately 2.4 million (Figure 1). It is the third largest city in the country. Cali is located in the middle of the Valley of the Cauca River, surrounded by the western and central branches of the Andes Mountains. The western area of Cali extends toward the mountains so that people in this area may live at altitudes as high as near 2,000 meters. The average annual precipitation varies between 900 mm3 and 1,800 mm3 and the average temperature is 24°C (74°F) with a range of 19°C to 30°C. Cali is divided into 21 localities (comunas) and has a well-organized healthcare system that takes into account the geographic location and socioeconomic status of its people as well as the complexity of their healthcare requirements. Adequate data were not available on exposure to feral cats, how well meat is cooked, or exposure to contaminated water.

Study population.

From July 22, 2005 to December 31, 2005, 955 pregnant women from 12 healthcare facilities were studied in an attempt to have representation from all geographical areas and socioeconomic strata in Cali. Serum from each of the patients was obtained from clinical blood samples already drawn for routine prenatal care in the ambulatory setting or for obstetric-related care in hospitalized patients. Women who had a suspected or confirmed diagnosis of T. gondii infection during pregnancy or toxoplasmosis prior to being enrolled in the study were excluded. We classified pregnant women into 3 socioeconomic strata (SES)—Low, Middle, and High—based on a classification of 6 social strata established by the Department of National Planning of Colombia. Low SES include persons living in poor communities in the urban and suburban areas belonging to strata 1 and 2; their households income is typically less than US $200 per month. Middle SES strata include persons living in urban and suburban areas belonging to strata 3 and 4; their household income ranges from US $200–$700/month. The high SES includes persons living in urban areas belonging to SE strata 5 and 6; their household income is typically greater than US $700/month.

Pregnant women suspected or confirmed to have acquired toxoplasmosis during gestation, as a result of this seroprevalence study, were treated by their own healthcare providers with spiramycin or pyrimetamine/sulfadiazine/folinic acid depending on their gestational age. Algorithm protocols for the management of toxoplasmosis during pregnancy were made available in Spanish to each of the 12 healthcare institutions when requested.

Serological detection of T. gondii infection.

Serum samples were tested for both IgG and IgM T. gondii antibodies by using a microparticle enzyme immunoassay (MEIA) method (Axsym System, Abbott Laboratories, Chicago, IL). These tests were performed at the Fundacion Valle del Lili (Cali, Colombia) per manufacturer’s instructions. All sera were tested after appropriate and written consent was obtained, placed at 4°C the day they were obtained and tested within one week. Results were made available to the patients’ physicians on a daily basis.

Statistical analysis.

Based on prevalence data obtained in the National survey study performed in 1980,12 a prevalence of 30–40% was expected. With this assumption and with a 95% confidence level, a sample size of at least 905 pregnant was estimated. Pregnant women were categorized by age and socioeconomic status; 3 age groups were established as follows: 14–19 years, 20–29 years, and 30–40 years; there were 3 socioeconomic status groups: Low, Medium, and High SES. Analysis for linear trends in the seroprevalence data was performed, P values less than 0.05 were considered to be statistically significant. Statistical analysis was performed using the Epi Info Version 3.3.2.

Institutional Review Boards (IRB) and Ethics Committees Approvals.

Independent IRB approvals were obtained from the 12 healthcare institutions in Cali, as well as from the Stanford University and Palo Alto Medical Foundation Research Institute IRBs in the United States. Informed consent was obtained from each woman in accordance with the decree N° 008430 of 1993 from the Ministry of Public Health of Colombia.

RESULTS

A total of 955 pregnant women were studied. The average age of these women was 25.1 years and the average gestational age was 23.8 weeks. Among these women, 437 were seropositive for Ig G antibodies (mean = 45.8%, 95% CI: 41.83–48.24%). Twenty-seven women were positive for IgM antibodies (2.8%, 95% CI 1.5–3.6%). The mean age of women with positive IgG titers was 26.1 years, and for seronegative women was 24.9 years (P = n.s.).

Seroprevalence increased significantly with increasing age (Table 1): 14–19 years: 39.0%, 20–29 years: 43.1%, and 30–39 years: 55.3% (χ2 for linear trend = 10.37 P = 0.00128). Stratified by their social and economic status (Table 2), the lower SE strata had the highest prevalence, 49%. The percentages in the other strata were: 38% for the middle SE strata and 29% for the high strata (χ2 for linear trend = 12.402, P = 0.0043). There was a significant increase in seroprevalence with increasing age within the lower SE strata: 14–19 years: 39.1%, 20–29 years: 48.3%, and 30–39 years: 63.2% (χ2 for linear trend = 9.53 P = 0.002). In the Middle SE strata there was a trend toward a higher prevalence with increasing age but it did not reach statistical significance: 36%, 34.0%, and 47.0% (χ2 for linear trend = 4.28 P = 0.07). In the Higher SE strata there was no significant change with increasing age (Figure 2).

Of the 27 patients who were positive by IgM antibodies, 23 had positive IgG and Ig M test results. Three had persistently negative IgG test results on serial testing after 3 weeks from the first sample and were considered to have false-positive IgM test results. One of the patients had an initial negative IgG result, but seroconverted later on a subsequent sample. During the study period a newborn of a mother in our study was diagnosed with severe congenital toxoplasmosis.

Pregnant women with positive IgG test results lived in all of the 20 localities of the city (Figure 3A). However, all pregnant women with positive IgM test results lived only in the East and West areas of Cali (the low and middle SE strata) (Figure 3B).

DISCUSSION

A wide variability in the prevalence rates of T. gondii seropositivity among pregnant women has been reported worldwide.1 A decrease in the prevalence of the infection over the past 25 years has been reported in developed countries (Table 3). In France the prevalence has declined from more than 80% during the 1960s to 54.3% in 1995.1,13 In Belgium, a major decrease was observed from 70% in 1966 to 47% in 1987.14 In the United Kingdom (South Yorkshire) a reduction was seen from 22% in 1969 to 8% in 1990.15 In the United States, several studies have shown a clear decrease in seroprevalence in several geographic locales (i.e., Palo Alto, California, from 24% in 1970 to 9% in 20031) and populations (in US military recruits has decreased by one third over the past 30 years from 14.4% to 9.5%3). The current overall and age-adjusted seroprevalence in the United States has been estimated to be between 13% and 18%.16

Although high prevalence rates have been reported from several Latin American countries including El Salvador,4 Costa Rica,5 and Brazil,6 data are limited regarding trends of T. gondii seroprevalence in this region. A recent experience in the central valley region of Costa Rica revealed a decrease in seroprevalence from more than 70% in the 1980’s to 58% in 2003.9

When our data was compared with those reported in the 1980 National Survey an increase in seroprevalence was noted in our population (Table 4). The observed seroprevalence in the 1980s in the population between 10 to 19 years and 30 to 39 yeas was 33.0% and 37.6%, respectively. Our study revealed a higher seroprevalence for these age groups: 39.0% and 55.3%, respectively (Table 1). These data suggest that transmission of T. gondii in the general population has been stable in some groups and localities over the past 3 decades whereas in others it appears to be increasing. Transmission may have occurred early in life (congenital or childhood) because at least 30% of the adolescent pregnant women (age group 10 to 19 years) were already infected. However, transmission appears to continue during adulthood.

Seroprevalence was higher in patients belonging to the lower SE strata suggesting that social and economic differences have a major impact on transmission of the parasite. Similar findings have been described in Brazil and Costa Rica.6,9 This increase was also related to age, except in the higher SE stratum in which the prevalence remained similar between the different age groups. Serologic test results suggestive of recent acquired infection (positive IgG and IgM titers) in our study were only found among women living in the lower and middle strata communities. This provides additional support for the presence of significant local risk factors for the transmission of the parasite in these socioeconomic groups at specific geographic locales (East and West areas of Cali).

Although the purpose of our study was to estimate the seroprevalence among pregnant women rather than to estimate the incidence of the infection during pregnancy, we did observe that 2.4% of women had both positive IgG and IgM antibodies. Of these women, one had recent seroconversion and the other gave birth to a newborn with congenital toxoplasmosis. Taken into account that not all women with positive IgG and IgM test results have a recently acquired infection, the incidence of acute infection during pregnancy in our study can be estimated approximately at 2–10/1.000 pregnancies, and of congenital toxoplasmosis, at least one neonate per 1.000 (0.1%). In Armenia, located in the Andes region of Colombia, the incidence of congenital toxoplasmosis has been estimated at 0.5%.17

Several factors may explain the fact that the seroprevalence of T. gondii infection in Cali has not decreased over the past 25 years or, in fact, may be increasing. In recent years, human migration (along with their domestic animals) to major cities in Colombia has significantly increased in part due to displacement of millions of people from rural areas due to decades of violence and the war on drugs.18 Several studies have shown that prevalence and transmission of T. gondii is higher in rural than in urban areas.15 Exposure to infected meat could be a risk factor as well but the convention in Colombia is to eat meat cooked to well done. Exposure to soil and water contaminated with cat’s feces are increasingly reported as being important in transmission to humans.19 We believe that our recent serological findings in Cali and the phenomenon of the “displaced” that affect so many Colombians belonging to the lower socioeconomic strata have created a highly dynamic situation for the circulation of the parasite in Cali. These findings are likely to be reproduced in other major urban areas. Further studies are warranted to define the mechanism by which T. gondii is transmitted in Cali.

Patients belonging to the lower SES groups had the higher prevalence rates of infection and the recent cases (positive IgG and IgM tests) were more commonly found in high-risk social and economically deprived areas (higher levels of poverty and of infant and maternal mortalities) defined by the Public Health Secretariat of Cali (http://planeacion.cali.gov.co/pot/propuesta/4-5.pdf) (Figure 3B).

Studies to determine the risk factors associated with the transmission of the parasite in other areas of Colombia have been performed. During the early 1980s, the national survey found no major differences in prevalence between women that lived with or without cats (41.6% versus 32.3%).12 In a recent case—control study in Armenia, Colombia the risk factors identified for pregnant women were contact with cats aged less than 6 months, eating undercooked meat, and drinking beverages prepared with un-boiled water.19 In recent years, the transmission due to contaminated water was identified as an important risk factor for transmission in certain areas of Canada and Brazil.6

A major concern is that most women in Cali are unaware of the risk factors for toxoplasmosis. Our group conducted a survey in pregnant women and found that 53% of them had not heard about toxoplasmosis. In addition, only 45% of these women could identify at least one way that they might prevent toxoplasmosis.20 Thus, major education efforts for primary prevention of T. gondii infection are needed in Cali.

Unlike other regions of the world where the prevalence for T. gondii infection has been declining over the past several decades, in Cali, Colombia, the prevalence appear to be increasing. Further studies are warranted to investigate the possible sources of infection and the health burden toxoplasmosis is imposing into the people of Cali.

Table 1

Seroprevalence of pregnant women in Cali, Colombia, stratified by age group

Age group (years)No. women (% positive)95% CI of seropositivity
* Comparison between age groups: χ2 for linear trend = 10.37 (P = 0.00128).
14–1995 (39.0%)32.0–46.6%
20–29573 (43.1)38.8–47.4%
30–40287 (55.3)*48.0–61.9%
Table 2

Seroprevalence of pregnant women in Cali, Colombia, stratified by Socio Economic Strata (SES)

Socioeconomic strata (SES)No. women (% positive)95% CI of seropositivity
* Comparison between SES groups: χ2 for linear trend = 12.402 (P = 0.0043).
Low573 (49)45.7–54.5%
Middle310 (38)31.6–44.0%
High72 (29)*15.6–55.3%
Table 3

Examples of decreasing prevalence of T. gondii antibodies in different geographical locales

Country, city or region*YearsSeropositivity (IgG)
* Bibliographic reference.
Switzerland, Geneva14197387%
198747%
France, Paris13196586%
199554%
UK, South Yorkshire15196922%
19908%
Sweden, Stockholm21196934%
198718%
Greece, Northern region22198437%
200424%
Poland, Lodz23199845.4%
200339.4%
US, Palo Alto1197024%
20039%
US recruits3196514.4%
19899.5%
Costa Rica, Central Valley region9198070%
200358%
Table 4

Comparison of T. gondii seroprevalence by age group between the general population of the western region of Colombia during 1980,12 and the pregnant women in Cali, Colombia during 2005

National survey (1980)12
10–19 years: 33.0%
20–29 years: 37.4%
30–39 years: 37.6%
Present study (2005)
14–19 years: 39.0%
20–29 years: 43.1%
30–39 years: 55.3%
Figure 1.
Figure 1.

Geographic localization of Colombia and of Cali, the largest city in the western region.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 78, 3; 10.4269/ajtmh.2008.78.504

Figure 2.
Figure 2.

Seroprevalence by age for the low, middle, and high socioeconomic strata (SES) and statistical trends within each SES: * in the low SES χ22) for linear trend = 9.53 P = 0.002, ** in the middle SES χ2 = 4.28 P = 0.07, *** in the high SES χ2 = 0.14 P = 0.704

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 78, 3; 10.4269/ajtmh.2008.78.504

Figure 3.
Figure 3.

Maps of Cali, Colombia: (A) Geographic distribution of pregnant women positive for IgG toxoplasma antibodies; (B) Individual women who had both IgG and IgM toxoplasma antibodies (black dots) shown in relation to social and economically deprived areas (See text).

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 78, 3; 10.4269/ajtmh.2008.78.504

*

Address correspondence to Fernando Rosso, Fundación Valle del Lili, Carrera 98 #18-49, Dirección Médica, Cali, Colombia, South America. E-mail: frosso07@gmail.com

Authors’ addresses: Fernando Rosso and José A. Chaves, Fundación Valle del Lili, Carrera 98 #18-49, Dirección Médica, Cali, Colombia, South America. Jessica T. Les, Stanford University School of Medicine, 300 Pasteur Dr., Stanford, CA 94305. Alejandro Agudelo, Carlos Villalobos, and Adriana Messa, Hospital Universitario del Valle, Departamento de Dynecologia y Obstetricia, Calle 5 #36-08, Cali, Colombia, South America. Gloria Anais Tunubala, Hospital Joaquín Paz Borrero, Carrera & ABis Calle 72, Cali, Colombia, South America. Jack S. Remington and José G. Montoya, Division of Infectious Diseases and Geographic Medicine, Stanford University School of Medicine, 300 Pasteur Dr., Stanford, CA 94305.

Acknowledgments: We are grateful to all the pregnant women who participated in the study. We also thank all the physicians, nurses, and healthcare providers in Cali who collaborated with our team at the different healthcare centers: Fundació n Clínica Valle del Lili : Martín Wartenberg, Betty Gómez, Ludwig Albornoz, Jaime López, Maria Fernanda Escobar, Alejandro Victoria, Marisol Badiel, Astrid Narváez. Hospital Universitario del Valle: Jorge Ivan Ospina, Laureano Quintero, Hoover Canaval, Alba Lucia Bohórquez. Comfenalco EPS: Vivian Rizo, Alvaro Alomia, Vivian Rizo, Juan Carlos Aristizabal, Maria Chois, Nancy Baltar. Coomeva EPS: Maria Elena Llanos, Angela Cruz, Julia Elena Martínez, Claudia Patricia Cataño, Jairo Guerrero. Comfandi EPS: Carlos Augusto Hernández, Ayde Quintero, Alfonso Recio. Hospital Isaias Duarte Cancino: Alejandro Varela. Hospital Primitivo Iglesias: Ricardo Gallego. Hospital Carlos Carmona: Elena Leonor Quinonez, Hospital Rafael Uribe-Uribe: Maria Cecilia Arturo, Hospital Carlos Holmes Trujillo: Jairo Arevalo Centro Medico Imbanaco: Gustavo Luna, Hoover Canaval, Blanca Garcia. Public heath secretariat of Cali: Nancy Aristizabal, Hector Fabio Cortes.

Dr. Rosso was beneficiary of a training grant by Fundacion Clinica Valle del Lili Cali, Colombia.

This study was presented in part at the International Conference on Women and Infectious Diseases satellite symposium during the 3rd International Conference in emerging infectious diseases. March 16–18, 2006, Atlanta, Georgia, United States.

REFERENCES

  • 1

    Remington JS, McLeod R, Thulliez P, Desmonts G, 2006. Toxoplasmosis. Chapter 31. In: JS Remington and J Klein, eds. Infectious Diseases of the Fetus and Newborn Infant (6th ed.). WB Saunders, Philadelphia, 947–1092.

  • 2

    Montoya JG, Liesenfeld O, 2004. Toxoplasmosis. Lancet 363 :1965–1976.

  • 3

    Smith KL, Wilson M, Hightower AW, Kelley PW, Struewing JP, Juranek DD, McAuley J, 1996. Prevalence of Toxoplasma gondii antibodies in US military recruits in 1989: comparison with data published in 1965. Clin Infect Dis 23 :1182–1183.

    • Search Google Scholar
    • Export Citation
  • 4

    Remington JS, Efron B, Cavanaugh E, Simon HJ, Trejos A, 1970. Studies on toxoplasmosis in El Salvador. Prevalence and incidence of toxoplasmosis as measured by the Sabin-Feldman dye test. Trans R Soc Trop Med Hyg 64 :252–267.

    • Search Google Scholar
    • Export Citation
  • 5

    Frenkel JK, 1980. Ruiz. Human Toxoplasmosis and cat contact in Costa Rica. Am J Trop Med Hyg 29 :1167–1180.

  • 6

    Bahia-Oliveira LM, Jones JL, Azevedo-Silva J, Alves CC, Orefice F, Addiss DG, 2003. Highly endemic, waterborne toxoplasmosis in north Rio de Janeiro state, Brazil. Emerg Infect Dis 9 :55–62.

    • Search Google Scholar
    • Export Citation
  • 7

    Neto EC, Anele E, Rubim R, Brites A, Schulte J, Becker D, Tuuminen T, 2000. High prevalence of congenital toxoplasmosis in Brazil estimated in a 3-year prospective neonatal screening study. Int J Epidemiol 29 :941–947.

    • Search Google Scholar
    • Export Citation
  • 8

    Glasner PD, Silveira C, Kruszon-Moran D, Martins MC, Burnier Junior M, Silveira S, Camargo ME, Nussenblatt RE, Kaslow RA, Belfort Junior R, 1992. An unusually high prevalence of ocular toxoplasmosis in southern Brazil. Am J Ophthalmol 114 :136–144.

    • Search Google Scholar
    • Export Citation
  • 9

    Zapata M, Reyes L, Holst I, 2005. Disminución en la prevalencia de anticuerpos contra toxoplasma gondii en adultos del valle central de Costa Rica. Parasitol Latinoam 60 :32–37.

    • Search Google Scholar
    • Export Citation
  • 10

    Gómez Marín JE, Castaño JC, Montoya MT, 1995. Toxoplasmosis congénita en Colombia: un problema subestimado de salud pública. Colomb Med 26 :66–70.

    • Search Google Scholar
    • Export Citation
  • 11

    Gomez JE, 1997. A maternal screening program for congenital toxoplasmosis in Quindio, Colombia and application of mathematical models to estimate incidences using age-stratified data. Am J Trop Med Hyg 57 :180–186.

    • Search Google Scholar
    • Export Citation
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    Juliao O, Corredor A, Moreno GS, Estudio Nacional de Salud: Toxoplasmosis en Colombia, Ministerio de Salud. Bogotá 1988; Imprenta Instituto Nacional de Salud

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