Antagonism between two intestinal parasites in humans: the importance of co-infection for infection risk and recovery dynamics

Abstract

Co-infection may affect transmission and recovery from infection, but remains an understudied element of disease ecology, particularly with regard to antagonism between parasites sharing a host. Helminth and giardia infections are often endemic in the same populations and both occupy the small intestine; yet few studies have examined interactions between these parasites. We report on helminth-giardia co-infections in a panel study of forager-horticulturalists in the Bolivian lowlands. Parasites were identified in faecal samples from 3275 participants, collected during 5235 medical exams over 6 years. Longitudinal co-infection patterns were examined using logistic mixed and multi-state Markov models. The most prevalent infections were hookworm (56%), Giardia lamblia (30%) and Ascaris lumbricoides (15%). Cross-sectionally, hookworm and A. lumbricoides were negatively associated with G. lamblia (OR = 0.60; OR = 0.65, respectively). Longitudinally, giardia infection was less likely in helminth-infected individuals (HR: 0.46). Infection with helminths was also less likely for individuals infected with giardia (HR: 0.71). Finally, treatment with mebendazole reduced subsequent hookworm infections, but resulted in a marginal increase in the odds of G. lamblia infection. Our results provide evidence for an antagonistic relationship between helminths and giardia, and suggest that co-infection should be considered in disease transmission models and treatment decisions.

Keywords: Bolivia; Tsimane; co-infection; giardia; helminths; state-based modelling.

Figures

Figure 1.

Prevalence of helminths and giardia. (a) Prevalences of giardia and helminths by study year. Both uncorrected prevalences (filled polygons) and prevalences corrected for age and village membership (dashed lines) are shown. (b) Total uncorrected infection prevalences for each species by 2-year age group. In both panels, prevalences are overlapping, not stacked. (Online version in colour.)

Figure 2.

Multi-state Markov models. (a,c) Arrows and values indicate the estimated instantaneous transition intensities between the possible states of uninfected (U), hookworm-infected (H), giardia-infected (G) and co-infected with both (C). (b,d) Examples of simulated 10-year infection histories for hookworm (lower, light bars) and giardia (upper, dark bars). (a,b) With no treatment, (c,d) with annual mebendazole treatment. (Online version in colour.)