Reduced cognitive function in children with toxocariasis in a nationally representative sample of the United States

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Abstract

Toxocariasis has recently been recognised as a potentially important neglected infection in developed countries, particularly those that experience substantive health disparities such as the United States. Given a relatively high prevalence of infection, an association between Toxocara infection and cognitive function may elucidate an important mechanism by which toxocariasis could contribute significantly to morbidity while still remaining hidden and, thus, neglected. To assess the potential relationship between toxocariasis and cognitive function, this investigation measured differences in components of both the Wechsler Intelligence Scale for Children-Revised (WISC-R) and the Wide Range Achievement Test-Revised (WRAT-R) in children seropositive and in children seronegative for Toxocara antibodies in the Third National Health and Nutrition Examination Survey, a large, nationally-representative survey of the United States population. Seropositive children scored significantly lower on the WISC-R and WRAT-R compared with the seronegative children. Moreover, this relationship was independent of socioeconomic status, ethnicity, gender, rural residence, cytomegalovirus infection and blood lead levels. These results identify an important association that may reflect morbidity attributable to a genuine neglected infection. Nevertheless, longitudinal data are required to confirm an etiological connection between toxocariasis and cognitive function, as well as the true population attributable risk for toxocariasis and its chronic sequelae.

Highlights

► Associations between infection with Toxocara spp. and cognitive function in children aged 6–16 years are reported. ► Infected children showed poorer cognitive function, even after adjustment for sociodemographics and blood lead levels.

Introduction

Despite adequate health resources, the United States continues to experience significant within-population disparity in health and morbidity (Adler and Rehkopf, 2008). Such disparities are often defined by the socioeconomics of ethnicity and poverty. Moreover, while the contributors to health disparity are multifaceted, neglected communities consistently manifest poorer health due to both chronic and infectious disease. Indeed, the distinctions between chronic and infectious disease may be difficult to distinguish, particularly with respect to the occurrence of what have been referred to as the neglected infections of poverty (Hotez, 2008). Neglected infections of poverty (NIP) are typically chronic infections, which often lead to chronic disease such as asthma, cardiovascular disease and poor cognitive development (Hotez, 2008, Hotez and Wilkins, 2009).

One such NIP in the United States is toxocariasis. It has been suggested that toxocariasis may represent the most important NIP in the United States (Hotez and Wilkins, 2009). Studies based on NHANES III have reported relatively high seroprevalence of Toxocara spp. antibodies (Won et al., 2008, Congdon and Lloyd, 2011). While the overall seroprevalence of Toxocara infection among all age groups was estimated at close to 14%, there were also marked differences across ethnic groups, with a seroprevalence of 21.2% among African-Americans, 10.7% among Mexican-Americans and 12.0% among Whites (Won et al., 2008). Most Toxocara infections are thought to be asymptomatic and acute complications, such as visceral or ocular larva migrans, rare. While acute complicated toxocariasis is indeed rare, this may not be the only relevant clinical presentation. Rather, more insidious chronic disease involving the lungs, vasculature and CNS may be more prevalent than previously expected and, thus, of greater public health significance (Hotez and Wilkins, 2009). With respect to neurological involvement, previous investigations have identified an inverse association between toxocariasis and cognitive function in children, wherein those infected with Toxocara spp. demonstrated poorer performance on multiple cognitive assessment instruments (Marmor et al., 1987, Nelson et al., 1996). Nevertheless, these studies were limited by small sample sizes (Marmor et al., 1987, Nelson et al., 1996) and incomplete control of confounding (Nelson et al., 1996).

To explore the possible relevance of toxocariasis as a neglected infection we sought to identify its association with cognitive function in children. This study tested the differences in two cognitive performance examination components between children with and without serological evidence of Toxocara spp. infection in a large representative sample of children living in the United States.

Section snippets

Survey and laboratory procedures

The relationship between Toxocara infection and cognitive function among US children was tested using data from NHANES III conducted between the years of 1988 and 1994 by the National Center for Health Statistics at the Centers for Disease Control and Prevention (CDC), USA. Methods describing this national survey have been reported previously (National Center for Health Statistics, US Department of Health and Human Services (DHHS). Third National Health and Nutrition Examination Survey,

Results

The overall prevalence of previous Toxocara infection among children aged 6–16 years in the NHANES III was 13.4%. Differences in sociodemographics, risk factors and measures of cognitive function are presented in Table 1. All four measures of cognitive function in math (P < 0.001), reading (P < 0.001), the block design performance (P < 0.001), and the verbal digit span (P < 0.001), were significantly reduced in children with previous Toxocara infection. The mean math and reading scores from the WRAT-R

Discussion

To the best of our knowledge, this is the first report of an association between Toxocara infection and childhood cognitive function in a nationally representative population-based sample of children in the United States. This investigation identified an independent inverse association between Toxocara infection and each of the four measures of cognitive function, wherein those with serological evidence of Toxocara spp. infection on average scored 0.76 points lower on the math test, 0.69 points

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    Citation Excerpt :

    While the full-expression syndromes of toxocariasis—visceral and ocular larva migrans—are relatively rare, there is an increasing evidence to link positive Toxocara serologies to human pulmonary and neurologic disease (Hotez and Wilkins, 2009; Ma et al., 2018). Pulmonary findings include asthma and lung dysfunction (Sharghi et al., 2001; Walsh and Haseeb, 2014), while neurologic disease ranges from epilepsy to cognitive delays (Hotez, 2014; Luna et al., 2018; Walsh and Haseeb, 2012). There is an urgent need to understand better the connections between serological diagnosis of human toxocariasis and these clinical findings, but if confirmed toxocariasis could be implicated as one of the most important human parasitic infections.

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