Toxoplasma gondii Infection in the United States, 1999–2004, Decline from the Prior Decade

Jeffrey L. Jones 0 1 Deanna Kruszon-Moran 0 1 Kolby Sanders-Lewis 0 1 Marianna Wilson 0 1 0 Diseases, National Center for Zoonotic , Vectorborne, and Enteric Diseases, CCID , Centers for Disease Control and Prevention , Mail- stop F-22, 4770 Buford Highway NE, Atlanta, GA 1 Division of Parasitic Diseases, National Center for Zoonotic , Vectorborne, and Enteric Diseases, CCID , Centers for Disease Control and Prevention, Atlanta, Georgia; Division of Health and Nutrition Examination Statistics, National Center for Health Statistics, Centers for Disease Control and Prevention , Hyattsville, Maryland Toxoplasma gondii can cause congenital, neurologic, ocular, and mild or asymptomatic infection. To determine the U.S. prevalence of T. gondii infection, we tested sera collected from the National Health and Nutrition Examination Survey (NHANES) 1999-2004 for T. gondii immunoglobulin G antibodies in persons 6-49 years old and contrasted the results to those comparable in NHANES III (1988-1994) (ages 12-49 years). Of the 17,672 persons examined in NHANES 1999-2004, 15,960 (90%) were tested. The age-adjusted T. gondii seroprevalence among persons 6-49 years old was 10.8% (95% confidence limits [CL] 9.6%, 11.9%), and among women 15-44 years old, 11.0% (95% CL 9.5%, 12.4%). T. gondii seroprevalence declined from 14.1% to 9.0% (P < 0.001) from NHANES III to NHANES 1999-2004 among U.S.-born persons ages 12-49 years. Although T. gondii infects many persons in the U.S., the prevalence has declined in the past decade. - Toxoplasma gondii is a nearly ubiquitous organism that infects humans, other mammals, and birds. However, only members of the cat family (Felidae) are the definitive host and shed the environmentally resistant oocyst form of the organism in their feces. Transmission to humans usually occurs by ingestion of cysts in undercooked meat and exposure to soil and water contaminated by oocysts. In rare cases, transmission by transfusion or organ transplantation has been reported. In general, humans are thought to be infected for life with cysts forming in the muscles, brain, and other organs, and IgG antibody production is thought to be lifelong. Human infections are usually asymptomatic or cause a selflimited illness with symptoms such as fever and lymph node enlargement. However, severe neurologic and ocular disease can occur with congenital infection and in immunesuppressed persons (usually reactivated disease). In addition, ocular disease has been estimated to occur in up to 2% of persons with normal immunity that are infected with T. gondii after birth.1 It is not yet known if chronic infection with T. gondii has other significant health-related consequences. Researchers are examining the effects of chronic T. gondii infection on reaction time,2 tendency for accidents,3 behavior,47 and mental illness.811 The prevalence of T. gondii varies greatly in populations throughout the world (from < 10% to > 90%) and is thought to be affected by food-production practices, water treatment, climate, topography, soil- and cat feces-related hygiene, occupational and non-occupational soil exposure, and culinary practices.1219 In the United States, there are an estimated 4004000 congenital infections per year,20 up to 1.26 million cases of ocular disease,1 and numerous cases of encephalitis and other systemic illnesses in immune-suppressed persons. Regardless of the source of infection, a reduction in the prevalence of T. gondii infection in the population will lead to many fewer cases of debilitating disease. In this study, we sought to determine the recent prevalence of T. gondii infec MATERIALS AND METHODS To monitor the prevalence of T. gondii infection in the United States, we tested sera collected in the National Health and Nutrition Examination Survey (NHANES) for the 6-year period from 1999 through 2004 and compared it to data from NHANES III (conducted from 1988 through 1994). The NHANES is a cross-sectional survey conducted by the National Center for Health Statistics (NCHS) based on a stratified, multistage probability cluster design from which a sample of the civilian, noninstitutionalized U.S. population is drawn. The NHANES collects representative health statistics on a variety of health measures and conditions through household interviews, standardized physical examinations, and collection of blood samples in mobile examination centers. Data has been collected continuously since 1999 and released in 2-year cycles. Non-Hispanic blacks, Mexican Americans, adolescents of age 1219 years, low-income persons, and persons age 60 and older are over-sampled to ensure adequate sample size. For the T. gondii antibody prevalence evaluation, we tested persons of age 649 years. Descriptions of the survey design and sampling methods have been published elsewhere.21,22 NHANES III and NHANES 19992004 were reviewed by the NCHS Institutional Review Board and included written informed consent. Variables used in data analysis were categorized as follows: age was grouped as 611, 1219, 2029, 3039, and 4049 years; however, in comparisons of NHANES 19992004 to NHANES III (19881994), the 611 year age group was excluded because a representative sample of sera for this age group was not available for testing for T. gondii in NHANES III. Race/ethnicity was defined by self-report as non-Hispanic White, non-Hispanic Black, or Mexican American. Persons who did not select one of these groups were categorized as Other and were only included when all racial/ethnic groups were combined. Poverty index was calculated by dividing the total family income by the U.S. poverty threshold, adjusted for family size. When comparing the NHANES III (19881994) prevalence to the NHANES 19992004 prevalence we examined only the U.S.-born population because this group more accurately represents transmission of T. gondii in the U.S. This is because in many countries outside the U.S., a relatively high percentage of persons are infected at an early age18,23 and therefore are already infected when immigrating to the U.S. A high prevalence of infection is found in many areas of Mexico and Latin America,18,23 and 65% of the NHANES 19992004 non-U.S.born persons ages 649 years are from Mexico. Programs designed to prevent T. gondii infection in the U.S. cannot be monitored accurately by evaluating the prevalence in foreignborn persons with the NHANES because of this high rate of infection that occurs before immigration. Laboratory testing. All serum samples were tested using the Platelia Toxo-G enzyme immunoassay kit (Bio-Rad, Hercules, California) according to the instructions provided by the manufacturer during each time period (as a result of the manufacturers testing and determination of threshold values for the kits, samples with > 6 IU were considered positive for T. gondii antibodies during the time of NHANES III,24 and samples with 10 IU were considered positive for T. gondii antibodies during the time of NHANES 19 (...truncated)