Individual predisposition, household clustering and risk factors for human infection with Ascaris lumbricoides: new epidemiological insights

Abstract

Background: Much of our current understanding of the epidemiology of Ascaris lumbricoides infections in humans has been acquired by analyzing worm count data. These data are collected by treating infected individuals with anthelmintics so that worms are expelled intact from the gastrointestinal tract. Analysis of such data established that individuals are predisposed to infection with few or many worms and members of the same household tend to harbor similar numbers of worms. These effects, known respectively as individual predisposition and household clustering, are considered characteristic of the epidemiology of ascariasis. The mechanisms behind these phenomena, however, remain unclear. In particular, the impact of heterogeneous individual exposures to infectious stages has not been thoroughly explored.

Methodology/principal findings: Bayesian methods were used to fit a three-level hierarchical statistical model to A. lumbricoides worm counts derived from a three-round chemo-expulsion study carried out in Dhaka, Bangladesh. The effects of individual predisposition, household clustering and household covariates of the numbers of worms per host (worm burden) were considered simultaneously. Individual predisposition was found to be of limited epidemiological significance once household clustering had been accounted for. The degree of intra-household variability among worm burdens was found to be reduced by approximately 58% when household covariates were included in the model. Covariates relating to decreased affluence and quality of housing construction were associated with a statistically significant increase in worm burden.

Conclusions/significance: Heterogeneities in the exposure of individuals to infectious eggs have an important role in the epidemiology of A. lumbricoides infection. The household covariates identified as being associated with worm burden provide valuable insights into the source of these heterogeneities although above all emphasize and reiterate that infection with A. lumbricoides is inextricably associated with acute poverty.

Figure 1. An illustration of the hierarchical structure of the data on Ascaris lumbricoides worm counts.

Participants live in households such that n_k participants live in household k and there are K households all together (K = 459, see main text “Sample Size, Data Structure and Missing Values”). The total number of participants is 1,795. Each participant contributes at most three measurements of worm burden, one after each round of chemo-expulsive treatment with pyrantel pamoate, and at least one measurement (after the first round of treatment). Participants who were not “satisfactorily de-wormed” (see main text “Sample Size, Data Structure and Missing Values”) at a given round of treatment were not subsequently followed up.

Figure 2. Mean worm burden at baseline vs. host age and sex.

Fitted points are posterior means calculated across all households from the “full” model (Model 1, see Table 3). Squares and solid lines denote males, circles and dashed lines females. Household risk factors are adjusted to their null levels, i.e. a Bangladeshi family of 2–4 sleeping members with no children, paying no rent, living in a house with a single room, an earth floor and private well and latrine facilities (see Table 4). Error bars represent 95% Bayesian credible intervals.

Figure 3. The proportion of the baseline mean worm burden after six months re-infection vs. host age.

Fitted points are posterior means estimated from the “full” model (Model 1, see Table 3). Squares and solid lines denote the first re-infection population, circles and dashed lines the second re-infection population. Error bars represent 95% Bayesian credible intervals.