Schistosomiasis's evolutionary response to a changing world - Can we keep up?
In an effort to unravel the complex transmission dynamics of zoonotic hybrid schistosomiasis, the Royal Veterinary College's Stefano Catalano, Anna Borlase and Elsa Leger, highlight some of the many components that could affect disease control and elimination programmes in West Africa.
From three years working on Schistosoma trematodes in Senegal and Niger as part of our ZELS project, we soon faced the continuously changing patterns of schistosomiasis disease in its endemic regions, with each study site bringing with it a new and intricate tale of people, livestock, and the wildlife that surrounds them. A constantly changing story of how each of these elements contributes to the transmission ofthesewaterborneparasites. In fact, while schistosomiasis is a well-known Neglected Tropical Disease (NTD), less understood is the presence of multiple, co-endemic Schistosoma species capable of exploiting a wide range of human and animal hosts.
With typical parasitic opportunism via zoonotic transmission, cross-species pairing, and hybridizations, schistosomes survive in a multi-host melting pot. For example S. mansoni, a causal agent for human intestinal schistosomiasis, has been shown to also thrive in rats and mice, and so does S. bovis, a parasite more typically found in cattle. In addition, complex hybridization dynamics between S. bovis and S. haematobium, which is responsible for human urogenital schistosomiasis, as between S. bovis and S. curassoni, a parasite of small ruminants, have expanded the host range that schistosomes are able to infect. This wider host spectrum has a significant and as yet underestimated impact on both human and livestock health.
Tackling such a multifaceted problem requires a multifaceted team. Within the ZELS project, medical and veterinary professionals, biologists, and educators have joined forces with the aim of improving our understanding of the distribution, impact, and opportunities for control of zoonotic hybrid schistosomes. Fieldwork in Senegal has involved sampling from livestock, wildlife, mollusc, and human populations, giving our multi-disciplinary team rare and often amusing insights into the challenges of each other’s sector.When faced with cattle that donot want to cooperate, technicians more used to school-based studies realised that obtaining urine and stool samples isnot always as simple as just distributing pots in the classroom, especially when those cattle have horns up to two-foot long! And so the need for a bespoke, innovative piece of equipment to facilitate animal sampling became apparent, and a selfie stick wired onto a specimen pot became the “bâton de pipi”. The seemingly endless days in the field and in the lab processing samples, collecting parasitic larvae for molecular typing…processing more samples… have all been made easier with the constant supply of hot sweet tea and immense hospitality of our Senegalese collaborators and the communities we worked with.
Through this research, the complexities of the hybrid schistosomiasis system in Senegal are only just starting to reveal themselves. What is clear is that wildlife, the environment, people, and their animals are all significant players. When resources are limited, as is so often the case with NTDs, it is natural to think “Why should we be worrying about animal disease rather than human disease? ”, but such a mind-set overlooks the reality in which many of these diseases exist.
The One Health concept, which provides the framework for our ZELS project, recognizes that human, animal, and ecosystem health are intricately interconnected. This is highly relevant for all NTDs and most evident in the case of neglected zoonotic diseases with a known animal reservoir, such as rabies. In other cases, the significance of animal reservoirs may not become apparent until a human epidemic occurs, or where human transmission is nearing elimination; in this case, Guinea-worm disease is a great example.18), 11:501-515.
Back to the zoonotic hybrid schistosomes encountered in both Senegal and Niger, we wonder whether this is a case of parasites and pathogens remaining one step ahead of us by rapidly evolving in the face of evolutionary pressures exerted by, for instance, disease eradication programmes. Or, in contrast, have there always been multi-host systems with an animal component and we have just never recognised them? Both scenarios should be considered when studying transmissible diseases in our changing world. This is especially true as conditions that often precede disease emergence, such as environmental changes due to deforestation and dam construction, are disproportionately borne by the same marginalized communities that are most affected by NTDs.
Such diseases impacting both humans and livestock often force a double burden on the communities that rely on animals for their livelihoods, with both public health challenges and veterinary issues (animal disease, death, sanctions, market closures, etc.). Identifying the best approaches and solutions to these complex situations often requires a cross-sector collaboration. It is true that multi-disciplinarity and inter-disciplinarity have become popular research buzzwords while the implementation of meaningful cross-disciplinary collaborations can be a challenging task. However, this has been one of the great successes of our ZELS project, with zoonotic schistosomiasis providing the perfect example of where a One Health framework has been absolutely necessary in order to understand the disease and to approach disease control.
Further resources
Research project: Epidemiology and evolution of zoonotic schistosomiasis in a changing world
Research article: One Health – an ecological and evolutionary framework for tackling Neglected Zoonotic Diseases .Evol. Appl. (2016), 9:313-333.
Research article: Should we be treating animal schistosomiasis in Africa? The need for a One Health economic evaluation of schistosomiasis control in people and their livestock. Trans. R. Soc. Trop. Med.Hyg. (2017), 111:244-247.
Research article: Rodents as natural hosts of zoonotic Schistosoma species and hybrids: an epidemiological and evolutionary perspective from West Africa. J. Infect. Dis. (2018), 218:429-433.
Research article: Introgressed animal schistosomes Schistosoma curassoni and S. bovis naturally infecting humans. Emerg. Infect. Dis. (2016), 22:2212-2214.
Research article: Opportunities and challenges for modelling epidemiological and evolutionary dynamics in a multihost, multiparasite system: zoonotic hybrid schistosomiasis in West Africa. Evol. Appl. (20