Spillover, hybridization, and persistence in schistosome transmission dynamics at the human-animal interface

Abstract

Zoonotic spillover and hybridization of parasites are major emerging public and veterinary health concerns at the interface of infectious disease biology, evolution, and control. Schistosomiasis is a neglected tropical disease of global importance caused by parasites of the Schistosoma genus, and the Schistosoma spp. system within Africa represents a key example of a system where spillover of animal parasites into human populations has enabled formation of hybrids. Combining model-based approaches and analyses of parasitological, molecular, and epidemiological data from northern Senegal, a region with a high prevalence of schistosome hybrids, we aimed to unravel the transmission dynamics of this complex multihost, multiparasite system. Using Bayesian methods and by estimating the basic reproduction number (R₀ ), we evaluate the frequency of zoonotic spillover of Schistosoma bovis from livestock and the potential for onward transmission of hybrid S. bovis × S. haematobium offspring within human populations. We estimate R₀ of hybrid schistosomes to be greater than the critical threshold of one (1.76; 95% CI 1.59 to 1.99), demonstrating the potential for hybridization to facilitate spread and establishment of schistosomiasis beyond its original geographical boundaries. We estimate R₀ for S. bovis to be greater than one in cattle (1.43; 95% CI 1.24 to 1.85) but not in other ruminants, confirming cattle as the primary zoonotic reservoir. Through longitudinal simulations, we also show that where S. bovis and S. haematobium are coendemic (in livestock and humans respectively), the relative importance of zoonotic transmission is predicted to increase as the disease in humans nears elimination.

Keywords: R0; hybrids; modelling; schistosomiasis; spillover.

Fig. 1.

Schematic of the multihost, multiparasite transmission model: S. haematobium, S. bovis, and Haematobium group hybrids in human and livestock populations. Parameter description and categorization of worm genotypes in definitive hosts are detailed in SI Appendix, Tables S1 and S2.

Fig. 2.

Longitudinal simulations under assumed current level of MDA with praziquantel (A: 50% annual coverage school-aged children) and under enhanced coverage (B: 90% annual coverage school-aged children). Mean worm burden in human population of S. haematobium, Hyb, F1 hybrids, and S. bovis under current level of zoonotic transmission and with no zoonotic transmission. Median shown as solid lines, dashed lines show 95% CIs.

Fig. 3.

Longitudinal simulations: Predicted impact of varied MDA coverage on proportion of worm burden in the human population that are hybrids under current level of zoonotic transmission (Left) and with no zoonotic transmission (Right).

Fig. 4.

The predicted impact on overall basic reproductive number (R₀^tot,Sb) for S. bovis of (A) annual treatment of the cattle population and (B) reducing the proportion of the cattle population contributing to schistosomiasis transmission. Solid blue lines indicate the median estimates from the uncertainty analysis and dashed blue lines indicate the 95% CIs.