Russell Stothard, LSTM and Janelisa Musaya, MLW
Our recent publication in One Health was the fruition of a two-year targeted disease surveillance programme across three districts of Malawi. Throughout, we harnessed our collaborative resources across our UK-USA-Malawi partnership and sought to answer this fundamental question: From where do hybrid human schistosomes originate?
The answer to such a simple question requires the collation of diverse facts, careful reasoning and time. This new scientific appraisal gives us both causal explanations and, importantly, permits sensible predictions. In this short blog, we describe how our team began to explore this human-animal-schistosomiasis interface.
Two decades ago, whilst with the Schistosomiasis Control Initiative (SCI), I (RS) first saw the close interactions between people, livestock and schistosomes. During our annual school-based epidemiological surveys on the shoreline of Lake Albert, Uganda, we were alarmed by the proximity that farmed animals shared with intense transmission foci of human schistosomiasis; we inspected local cattle. There, we described bovine schistosomiasis, viz. Schistosoma bovis, hitherto unknown locally, existing alongside an intestinal schistosomiasis, viz. Schistosoma mansoni, focus.
Though the genetic divergence between S. bovis and S. mansoni was too significant for natural hybridisation to occur in humans or cattle, some five years later, in a similar lakeshore setting in Senegal, we demonstrated the genetic distance between S. bovis and S. haematobium, viz. urogenital schistosomiasis, was within the species-specific boundaries for schistosome evolution to occur by hybridisation. This seminal insight into schistosome reproductive biology surprised many and even unsettled some.
The ability to track S. haematobium-bovis variants with molecular assays within any infected host, albeit humans and or animals, exposed a rich seam of later research.
This incrementally evidenced that urogenital schistosomiasis was caused by parasites that had, and were having, a growing connection with livestock. If such parasites could successfully sustain themselves in environmental transmission outside an exclusive need for human hosts, these will continue to enter into human transmission cycles.
Since then, S. haematobium-bovis hybrids have dispersed out of Africa to spark novel transmission foci elsewhere, the most important of which was to establish urogenital schistosomiasis on the Mediterranean island of Corsica. This hybrid combination first piqued our interest in Malawi in 2018, being found well outside of its previously reported range in western and northern Africa. It was here that we also encountered another hybrid variant, S. haematobium-mattheei. The latter arises from another schistosome species found within the southern cone of Africa.
Having at least two hybrid variants circulating in people and not knowing where they were coming from kindled our urge to highlight these biological unknowns in “Future schistosome hybridisations: Will all Schistosoma haematobium hybrids please stand up?” It was a general alert to the disease control community to consider the growing importance of One Health aspects of urogenital schistosomiasis.
From April 2021, the Wellcome Trust funded HUGS “hybridisation in urogenital schistosomiasis” commenced. After that, Janelisa and I, with our newly recruited LSTM-MLW staff, developed a formal surveillance framework to survey livestock. We used a novel combination of miracidial hatch tests on faecal samples and carcass dissection methods to collect adult worms from slaughtered livestock. We then examined all collected schistosome material with molecular assays to reveal their genetic identities, see images H to K.
The upshot was that cattle in Malawi can harbour S. haematobium-mattheei but strangely not S. haematobium-bovis hybrids and a smaller minority of animals are infected with S. haematobium itself. The latter was the first time this species was found in cattle. We can now conclude that hybrid S. haematobium-mattheei schistosomes are regularly.
Looking ahead with further expansion in cattle production locally and their unregulated movements within areas where urogenital schistosomiasis occurs, it is safe to assume the rate at which hybrid schistosomes will enter human transmission cycles will increase. To counter this phenomenon, it is now essential to consider practical strategies and appropriate interventions for disease control in cattle to diminish the entry of hybrids into general environmental transmission.
Our newest publication lays a solid foundation for a better understanding the One Health of urogenital schistosomiasis. In February 2025, we will consolidate these findings by hosting a scientific meeting of the Royal Society to discuss the importance of hybrid schistosomes in Africa and beyond.