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    Percentage of Toxoplasma gondii antibody-positive persons among Toxocara spp. antibody-positive and Toxocara spp. antibody-negative persons in the United States, Third National Health and Nutrition Examination Survey (1988–1994) (n = 16,646).

  • View in gallery

    Percentage of Toxocara spp. antibody-positive persons among Toxoplasma gondii antibody-positive and Toxoplasma gondii antibody-negative persons in the United States, Third National Health and Nutrition Examination Survey (1988–1994) (n = 16,646).

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Toxoplasma gondii and Toxocara spp. Co-infection

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  • 1 Division of Parasitic Diseases, National Center for Zoonotic, Vectorborne, and Enteric Diseases, Coordinating Center for Infectious Diseases, 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 and Toxocara spp. infections can cause systemic and ocular disease. To estimate the prevalence of infection with these organisms, we tested serum samples from persons ≥ 12 years of age obtained in the Third National Health and Nutrition Examination Survey (1988–1994). Among those tested for both T. gondii and Toxocara spp. (n = 16,646), the age-adjusted T. gondii antibody prevalence was 23.6% (95% confidence limit [CL] = 22.1–25.1%) and the Toxocara spp. antibody prevalence was 14.0% (95% CL = 12.7–15.4%). Multivariate analysis controlling demographic and risk factors showed that persons infected with Toxocara spp. were more likely to be infected with T. gondii (odds ratio [OR] = 1.93, 95% CL = 1.61–2.31), and similarly, persons infected with T. gondii were more likely to be infected with Toxocara spp. (OR = 1.91, 95% CL = 1.59–2.28). Infection with T. gondii and Toxocara spp. are common and can be prevented by many similar interventions.

INTRODUCTION

Toxoplasma gondii and Toxocara spp. infections, which can cause systemic and ocular disease, share soil ingestion as a common mode of exposure. Toxoplasma gondii, a protozoan parasite, is shed as environmentally resistant oocysts in cat feces and becomes infectious after 1–5 days when the oocysts sporulate.1 Oocysts can remain infectious for months to years.2,3 Contaminated soil ingestion is one of the principal modes of human infection with T. gondii.4 If a pregnant woman becomes newly infected with T. gondii, congenital infection can occur and may lead to neurologic or ocular disease (retinitis) in the fetus. In addition, up to 2% of humans infected with T. gondii after birth develop ocular disease.5

Toxocara canis and Toxocara cati are nematode parasites of dogs and cats, respectively. The adult stages of Toxocara spp. reside in the small intestine of dogs and cats where they oviposit; eggs are then shed in the feces where they embryonate and become infectious after several weeks in the environment.6 Toxocara spp. eggs can remain viable in the soil for months to years.6 When humans ingest infective eggs of Toxocara spp. from contaminated soil, the larva are released, penetrate the gut wall, and then migrate through the internal organs. The larvae do not usually undergo any further development in humans. If a sufficient number of larvae are present, they can cause severe local reactions that clinically are termed visceral larva migrans and are associated with eosinophilia, hepatosplenomegaly, hyperglobulinemia, pulmonary symptoms, and fever. Migration of even a single larva to the retina (ocular larva migrans), can lead to loss of vision in the affected eye.68

Because T. gondii and Toxocara spp. share soil ingestion as a common mode of exposure, we postulated that infection with one of these organisms would be associated with an increased risk for infection with the other. Using a national survey, we determined the prevalence of antibodies to T. gondii and Toxocara spp. and examined risk factors for co-infection with these organisms.

MATERIALS AND METHODS

To determine the prevalence of IgG to T. gondii and Toxocara spp., we tested serum from the Third National Health and Nutrition Examination Survey (NHANES III), a cross-sectional survey conducted between 1988 and 1994 by the National Center for Health Statistics of the Centers for Disease Control and Prevention (CDC). NHANES III was designed to obtain nationally representative statistics on health measures and conditions through household interviews, standardized physical examinations, and collection of blood samples in mobile examination centers.9 This survey was based on a stratified, multistage, probability cluster design from which a sample representative of the civilian, noninstitutionalized U.S. population ≥ 2 months was drawn. Non-Hispanic Blacks, Mexican-Americans, children 2 months through 5 years of age, and persons ≥ 60 years of age were sampled at higher rates than other persons to ensure an adequate sample size for these groups. Detailed descriptions of the design of the survey and the sample have been published elsewhere.9 NHANES III was reviewed and approved by a human subjects review committee at CDC.

Surplus sera for persons ≥ 12 years of age were available for testing for antibodies to T. gondii and Toxocara spp. Sera were also available and tested for a limited number of children 1–5 and 6–11 years of age. Because of the limited availability of sera from children, estimates from these age groups have a great potential for bias and inferences should not be made for the nation. However, for completeness we present limited data for children < 12 years of age in the results.

For the principal analysis, age was grouped as 12–19, 20–29, 30–39, 40–49, 50–59, and ≥ 60 years. Race/ethnicity, based on self-reported information, was categorized as non-Hispanic White, non-Hispanic Black, or Mexican-American. Those who did not self select as non-Hispanic white, non-Hispanic black, or Mexican-American were placed in the “other” racial/ethnic group. Poverty index was calculated by dividing the total family income by the U.S. poverty threshold, adjusted for family size. Crowding index was calculated by dividing the number of household residents by the total number of rooms in a household (excluding bathrooms) and was expressed as the number of persons per room (categorized as < 0.5, 0.5–0.99, and ≥ 1.0 persons per room). Education was measured as the last year of schooling completed by the head of household and grouped into three levels (less than high school, high school completed, and some college or college graduate). Metropolitan residence was defined as residence in a central metropolitan county with a population ≥ 1 million; residence in all other counties (including rural areas) was defined as non-metropolitan residence. High blood lead level was defined as ≥ 10 μg/dL. Dog and cat ownership were defined as ownership at the time of the survey.

Laboratory testing.

Specimens were tested for IgG to T. gondii using the Patelia Toxo-G immunoglobulin G enzyme immunoassay (Bio-Rad, Hercules, CA) according to the manufacturer’s instructions. Results were measured in international units (IU), with samples > 6 IU considered positive for IgG to T. gondii. Prior to the study the Patelia Toxo-G kit was evaluated by comparison with the CDC Toxoplasma immunofluorescence assay-immunogloblin G test and the Sabin-Feldman dye test (obtained from Jack Remington, Palo Alto, CA) and found to have a sensitivity and specificity of 100%.10

For Toxocara spp., all specimens were tested using a CDC in-house enzyme immunoassay (EIA). The standard Toxocara spp. test used at CDC is a serial dilution EIA with results reported as a titer, and has sensitivity of 78% and a specificity of 92%.11 However, because of the limited volume of samples tested for NHANES III, using the serial dilution test was not practical, and it was necessary to use a one dilution test. An assessment of the one dilution test with 25 positive and 24 negative samples at CDC determined that the sensitivity and specificity was approximately the same as the serial dilution test (96% and 100%, respectively, comparing the one-dilution EIA with the standard serial dilution EIA). The test does not distinguish between the two species of Toxocara canis and Toxocara cati.

Statistical analysis.

Prevalence estimates were weighted to represent the total U.S. population and to account for over-sampling and nonresponse to the household interview and physical examination.12,13 Estimates were age-adjusted by the direct method to the 2000 U.S. population. Statistical analyses were conducted with SUDAAN, a family of statistical procedures for analysis of data from complex sample surveys.14 Standard error estimates were calculated using the Taylor series linearization method. Multivariate logistic regression was used to determine the independent predictors of T. gondii, Toxocara spp., and co-infection seropositivity with a P value < 0.05 from a Satterthwaite adjusted F-statistic considered significant.

RESULTS

Of 27,145 persons sampled for NHANES III, 22,266 (82%) persons ≥ 12 years of age were interviewed. Of these persons, 20,241 (91%) underwent physical examinations and 16,646 (82%) of the examined persons had surplus sera available and were tested for both antibodies to T. gondii and Toxocara spp. The availability of specimens for antibody testing among those examined varied by age (12–19 years of age [78%], 20–29 years of age [82%], 30–39 years of age [83%], 40–49 years of age [84%], 50–59 years of age [88%], 60–69 years of age [87%], and ≥ 70 years of age [79%]), race/ethnicity (non-Hispanic blacks [81%], non-Hispanic whites [83%], Mexican-Americans [83%]), sex (females [80%] and males [85%]), metropolitan residence (metropolitan [81%] and non-metropolitan [84%]), birth origin (foreign born [81%] and U.S. born [83%]), region (northeast [78%], west [78%], south [84%], and midwest [85%]), crowding (> 1 person per room [80%], 0.5–0.99 persons per room [82%], and < 0.5 person per room [84%]) (P < 0.05), but did not vary with respect to poverty index, head of household education level, or dog or cat ownership.

As noted in the Materials and Methods, the availability of sera for children < 12 years of age was limited. Among children 1–5 years of age, 729 (9.4%) of those examined were tested for antibodies to T. gondii and Toxocara spp. Among children 6–11 years of age examined, 1,598 (48.6%) were tested for antibodies to T. gondii and Toxocara spp.

Among persons ≥ 12 years of age, the overall age-adjusted T. gondii seroprevalence was 23.6% (95% confidence limit [CL] = 22.1–25.1%), and the overall age-adjusted Toxocara spp. prevalence was 14.0% (95% CL = 12.7–15.4%). For persons with antibodies to Toxocara spp. (n = 2,640), the age-adjusted T. gondii prevalence was 35.5% (95% CL = 32.6–38.5%). For persons negative for antibodies to Toxocara spp. (n = 14,006), the age-adjusted T. gondii prevalence was 21.7% (95% CL = 20.1–23.2%). Figure 1 shows the T. gondii antibody prevalence by age group among persons positive for antibodies to Toxocara spp. and negative for antibodies to Toxocara spp.

Among persons with antibodies to T. gondii (n = 4,240), the age-adjusted Toxocara spp. prevalence was 22.3% (95% CL = 20.0–24.6%). Among persons negative for antibodies to T. gondii (n = 12,406) the age-adjusted Toxocara spp. prevalence was 11.7% (95% CL = 10.4–13.1%). Figure 2 shows the Toxocara spp. antibody prevalence by age group among persons positive for antibodies to T. gondii and negative for antibodies to T. gondii. Children 12–19 years of age who were infected with T. gondii were especially likely to be infected with Toxocara spp. (28.9%, 95% CL = 20.7–37.1%).

Because of the low availability of serum from children 1–5 years of age tested for antibodies to T. gondii and Toxocara spp. (9.4%), proportions derived from these numbers are not statistically reliable or generalizable, However, among these 729 children, 30 were positive for T. gondii, 58 to Toxocara spp., and only 5 to both species. Because of the limited availability of sera from children 6–11 years of age (48.6%), these samples cannot be treated as a nationally representative sample of this age group. Inferences should not be made to a national total because the potential for bias is great when response is this low. However, unweighted estimates of antibody seropositivity among children 6–11 years of age were 5.8% to T. gondii, 15.1% to Toxocara spp., and 1.8% to both species.

Multivariate analysis showed that having antibodies to one organism nearly doubled the odds of having antibodies to the other organism (persons infected with Toxocara spp. were more likely to be infected with T. gondii (odds ratio [OR] = 1.93, 95% CL = 1.61–2.31), and persons infected with T. gondii were more likely to be infected with Toxocara spp. (OR = 1.91, 95% CL = 1.59–2.28) (Table 1). Other risk factors for T. gondii seropositivity, Toxocara spp. seropositivity, and co-infection are shown in Table 1. The odds ratio for co-infection was higher in those ≥ 20 years of age than those 12–19 years of age, males than females, persons living in non-metropolitan than metropolitan areas, foreign born than U.S. born persons, persons living below the poverty level than those at or above the poverty level, those whose head of household had less than a high school education than those with more than a high school education, and persons who were dog owners than those that did not own dogs. The OR for co-infection was lower among Mexican-Americans than non-Hispanic whites, and lower in the west than in other regions of the United States (Table 1).

DISCUSSION

In this seroprevalence study of a representative sample of the U.S. population, we found that for the parasitic organisms T. gondii and Toxocara spp., infection with one organism (as indicated by IgG) is associated with nearly twice the risk of infection with the other organism. Toxoplasma gondii and Toxocara spp. are very different parasites, one a protozoan and the other a helminth, and during evaluation of the Toxocara spp. serologic EIA there was no evidence of cross-reaction.11 Because both organisms share contaminated soil ingestion as a common mode of exposure, our risk findings are plausible. Cats and dogs both defecate in soil and humans ingest soil though pica behaviors, especially during childhood, or inadvertently when soil gets on their hands during work or play. Studies have shown that soil in public parks and private backyards is often contaminated with Toxocara spp. eggs,6,15,16 and gardening, soil contact, and poor hand hygiene have been found to be risk factors for T. gondii infection.1719

Toxoplasma gondii generally infects humans for life, and the antibody response is thought to persist throughout life.20 Although toxoplasmosis-associated ocular disease is more common in the months after acute infection, it may occur after many years.5 Toxocara spp. are thought to migrate for months in humans and then lodge in host tissues in a state of arrested development. Toxocara-related ocular disease can occur months to years after the initial infection.6 Although most persons with visceral larva migrans and ocular larva migrans have antibody responses for 2–3 years,21 we are not aware of studies that evaluated the duration of Toxocara spp. antibody response over many years. Toxocara spp. antibody prevalence did not increase with age (Figure 2), and therefore more years for potential exposure, which suggests that the Toxocara spp. immune response may wane over time. However, because this is a cross-sectional study, people may have been infected primarily when they were young, and younger persons may have been as likely to be exposed to Toxocara spp. in recent years as older persons were when they were young.

In contrast to the Toxocara spp. antibody prevalence age profile, T. gondii antibody prevalence increases with age (Figure 1). However, T. gondii has another common mode of transmission, undercooked meat, and seroreactivity to T. gondii is known to be long lasting. In addition to soil exposure, it is likely that humans have more chances to be exposed to T. gondii through ingestion of undercooked meat as they age. Alternatively, it has been documented that T. gondii is less common in undercooked meat such as pork in recent years,22 and older persons may have been more likely to have been exposed to T. gondii in undercooked meat when they were young.

Our seroprevalence survey is subject to several limitations. In NHANES III, race/ethnicity, birth origin, and socioeconomic data were self-reported and not verified by independent methods. In addition, NHANES III was designed to collect information on a wide variety of risk factors for chronic diseases rather than the seroprevalence of antibodies to T. gondii and Toxocara spp. Surplus serum samples were not available for everyone examined and, as noted above, only a limited number of samples were available for children less than 12 years of age. Although the sensitivity and specificity were high for the T. gondii EIA (100%), they were not as high for the Toxocara spp. EIA (78% and 92%, respectively). Some false-negative and false-positive Toxocara spp. results are expected to have occurred. Although sensitivity and specificity for the Toxocara spp. assay were not optimally high, tests using the antigen in our study are considered to be useful in non-tropical areas where infection with other helminthes that might cross-react is less likely. For populations from tropical areas, recombinant antigens have been used to increase specificity.23,24

The risks for T. gondii, Toxocara spp., and coinfection seropositivity were lowest in the western United States (Table 1). The lower risk for seropositivity in the west may be caused by the more arid climate; both T. gondii and Toxocara spp. are susceptible to drying.6,25 The risks for T. gondii, Toxocara spp., and coinfection seropositivity were also greater when the head of the household had less than a high school education, which may be caused by more soil contact with manual labor or more frequent exposure to contaminated environments. It is interesting to note that although foreign born persons overall had a higher risk for seropositivity, Mexican-Americans as a group had a lower risk. This finding may be caused by the fact that most (55.3%) Mexican-Americans in the United States live in the more arid western United States.26

With an estimated 73 million dogs and 90 million cats27 in the United States, there is potential for widespread environmental contamination with T. gondii and Toxocara spp. Guidelines for prevention of T. gondii and Toxocara spp. infections have been published by CDC,28,29 the American Association of Veterinary Practitioners,29 and the Companion Animal Parasite Counsel.30 According to these guidelines, to prevent T. gondii environmental contamination, cats should be kept indoors, not allowed to hunt, and not be fed undercooked meat.28 Humans can prevent soil-related T. gondii infection by washing their hands after gardening or soil exposure, covering sand boxes, and washing fruits and vegetables that are eaten raw and may be contaminated with soil. To prevent Toxocara spp. environmental contamination, dogs and cats should be de-wormed appropriately,29,30 dogs kept on a leash, and dog feces cleaned up. In addition, dogs and cats should be excluded from portions of parks and playgrounds frequently used by children. These measures should help prevent human morbidity caused by these two disparate, yet highly adaptive parasites.

Table 1

Risk factors for seropositivity to antibodies to Toxoplasma gondii and Toxocara spp. and seropositivity to both organisms (co-infection) calculated with multiple logistic regression, among persons ≥ 12 years of age, Third National Health and Nutrition Examination Survey, 1988–1994, n = 16.646*

CharacteristicT. gondii odds ratio95% Confidence limitsToxocara spp. odds ratio95% Confidence limitsCo-infection odds ratio95% Confidence limits
* NA = not applicable in this model; Ref = reference group.
P < 0.05 from Satterthwaite adjusted F-statistic in multivariate logistic model.
T. gondii antibody positive
    YesNA1.9†1.6–2.3NA
    NoRef
Toxocara antibody positive
    Yes1.9†1.6–2.3NANA
    NoRef
Age groups, years
    ≥ 607.9†5.6–11.20.80.7–1.14.0†2.6–6.1
    40–594.4†3.3–5.90.80.6–1.12.5†1.5–3.9
    20–392.0†1.4–2.71.10.9–1.41.7†1.0–2.7
    12–19RefRefRef
Race/ethnicity
    Mexican-American0.80.7–1.00.6†0.4–0.80.6†0.4–0.9
    Non-Hispanic Black1.00.8–1.21.7†1.4–2.01.30.9–1.8
    Non-Hispanic WhiteRefRefRef
Sex
    Male1.10.9–1.31.5†1.3–1.81.7†1.4–2.1
    FemaleRefRefRef
Metropolitan area
    Non-metropolitan1.10.9–1.31.4†1.1–1.71.5†1.1–2.0
    Metropolitan ≥ 1 million personsRefRefRef
Birth origin
    Not U.S. born2.1†1.8–2.61.6†1.2–2.42.7†1.7–4.4
    U.S. bornRefRefRef
Census region
    Northeast1.9†1.4–2.72.1†1.3–3.23.5†2.3–5.2
    Midwest1.4†1.1–1.71.6†1.0–2.51.7†1.1–2.7
    South1.3†1.1–1.72.1†1.4–3.12.2†1.5–3.3
    WestRefRefRef
Poverty index
    Below1.10.9–1.31.4†1.2–1.81.5†1.0–2.1
    At or aboveRefRefRef
Crowding index, persons/room
    ≥ 11.20.9–1.51.20.8–1.91.50.9–2.4
    0.5–0.991.00.8–1.21.00.8–1.20.90.7–1.2
    < 0.5RefRefRef
Head of household education
    Less than high school1.6†1.4–1.92.1†1.7–2.62.3†1.7–3.1
    High school1.3†1.0–1.61.5†1.2–1.81.31.0–1.7
    More than high schoolRefRefRef
High lead level (≥ 10 μg/dL)
    YesNA1.41.0–1.91.51.0–2.2
    NoRefRef
Dog owner
    YesNA1.2†1.0–1.31.6†1.3–2.2
    NoRefRef
Cat owner
    Yes1.10.9–1.31.21.0–1.51.10.8–1.6
    NoRefRefRef
Figure 1.
Figure 1.

Percentage of Toxoplasma gondii antibody-positive persons among Toxocara spp. antibody-positive and Toxocara spp. antibody-negative persons in the United States, Third National Health and Nutrition Examination Survey (1988–1994) (n = 16,646).

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 78, 1; 10.4269/ajtmh.2008.78.35

Figure 2.
Figure 2.

Percentage of Toxocara spp. antibody-positive persons among Toxoplasma gondii antibody-positive and Toxoplasma gondii antibody-negative persons in the United States, Third National Health and Nutrition Examination Survey (1988–1994) (n = 16,646).

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 78, 1; 10.4269/ajtmh.2008.78.35

*

Address correspondence to Jeffrey L. Jones, Division of Parasitic Diseases, National Center for Zoonotic, Vectorborne, and Enteric Diseases, Coordinating Center for Infectious Diseases, Centers for Disease Control and Prevention, 4770 Buford Highway NE, Mailstop F-22, Atlanta, GA 30341-3724. E-mail: jlj1@cdc.gov

Authors’ addresses: Jeffrey L. Jones, Division of Parasitic Diseases, National Center for Zoonotic, Vectorborne, and Enteric Diseases, Coordinating Center for Infectious Diseases, Centers for Disease Control and Prevention, 4770 Buford Highway NE, Mailstop F-22, Atlanta, GA 30341-3724, E-mail: jlj1@cdc.gov. Deanna Kruszon-Moran, Division of Health Examination Statistics, National Center for Health Statistics, Centers for Disease Control and Prevention, HYAT Building IV, Room 4308, Mailstop P08, Hyattsville, MD 20782, E-mail: ddk0@cdc.gov. Kimberly Won, Marianna Wilson, and Peter M. Schantz, Division of Parasitic Diseases, National Center for Zoonotic, Vectorborne, and Enteric Diseases, Coordinating Center for Infectious Diseases, Centers for Disease Control and Prevention, Mailstop F-36, 4770 Buford Highway NE, Atlanta, GA, E-mails: kfw7@cdc.gov, myw1@cdc.gov, and pms1@cdc.gov

Acknowledgments: We thank David Stansfield for his interest in and assistance with the study.

Financial support: This study was supported in part by a grant from Novartis Animal Health USA, Inc.

Disclaimer: The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the Department of Health and Human Services or the Centers for Disease Control and Prevention.

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