Population Genetics of Bovine and Human Schistosomes in Côte d'Ivoire

Neglected tropical diseases (NTDs) are a diverse group of infectious disease that severely affect the health of over one billion people in 149 countries across the globe. Schistosomiasis and fascioliasis are among the 20 NTDs identified by the World Health Organization (WHO) and are identified for control in the WHO’s Roadmap, Ending the neglect to attain the sustainable development goals: A road map for neglected tropical diseases 2021-2030.
These two NTDS caused by trematode parasites, are also classified as zoonotic neglected tropical diseases and are, therefore, not only of great concern to human health professionals but also to veterinary health professionals, as they cause considerable human morbidity and economic loss to the livestock industry. Furthermore, as these are diseases of poverty, their endemicity in low-resource settings endanger the attainment of United Nation’s Sustainable Development Goal number one: end poverty.
Many resources are devoted to the control and prevention of human fascioliasis and schistosomiasis and, while these programs have had success, continuous adaption of the parasites to evade control measures is a constant risk. Hybridization of species is an opportunity for organisms to acquire advantageous traits. In the case of parasites, examples include expanded host range and increased pathogenicity. To date numerous combinations of schistosome species from livestock and humans, as well as Fasciola hybrids have been documented. In the context of NTD control, hybridization poses a threat to expensive gains made by control and prevention programs, especially if it leads to persistent animal reservoirs or drug resistance.
Population genetics offers insight into genetic diversity, population structure and gene flow, which influence how alleles spread throughout a population. Understanding the extent of, and barriers to gene flow can help forecast the direction and rate of spread of advantageous alleles such as drug-resistance and inform efforts to reduce this risk.
This project used a One Health approach to examine transmission dynamics and hybridization of human and animal trematodes in sub-Saharan Africa. One Health is a holistic approach to health that addresses the links between human and animal medicine, public health and environmental sustainability for the betterment of the health and well-being of humans, animals and the environment. It emphasizes transdisciplinarity, collaboration and systems thinking and is particularly useful when tackling control of zoonotic diseases.
The aims of this thesis were to identify Schistosoma and Fasciola species found in Ivorian humans, cattle, sheep and goats using mitochondrial and nuclear loci, quantify genetic diversity and infer transmission dynamics of schistosomes within and between definitive hosts and geographical locations in Côte d’Ivoire. In addition to these aims, the sensitivity of the sedimentation method for diagnosis of cattle schistosomiasis was assessed and a clinical trial testing the effectiveness of triclabendazole in Fasciola infected Ivoirian cattle was conducted.
In order to meet these goals Schistosoma and Fasciola flukes from slaughtered cattle, sheep and goats at five abattoirs across Côte d’Ivoire were collected. Additionally, Schistosoma miracidia were hatched from the urine of humans and feces of cattle, sheep and goats in villages and farms sharing the same water source in Northern Côte d’Ivoire. DNA was extracted from all biological samples for genetic analysis of mitochondrial and nuclear loci as well as microsatellites.
High prevalences of schistosome hybrids were observed in humans in Côte d’Ivoire. Various degrees of hybridization were observed, indicating that this region is a stable hybrid zone. It would appear that most hybrids are a cross between human (Schistosoma haematobium) and livestock species (S. bovis), however, in the North we observed traces of S. curassoni (a schistosome species of livestock) in hybrids, indicating that S. curassoni may also play a role in human schistosomiasis. Cattle did not harbour any hybrids, and all cattle across the five sites were infected with S. bovis.
Schistosomes in Côte d’Ivoire were genetically diverse across all locations. Geographical structuring was observed in human schistosome populations, while cattle schistosome populations appear to be panmictic, with very little structuring.
The molecular investigation of Fasciola flukes from Chad and Côte d’Ivoire revealed the first Fasciola hybrid (F. gigantica x F. hepatica) in Africa, from Chad, and a clinical trial demonstrated that triclabendazole is an effective treatment for Fasciola infected Ivorian cattle.
Observations during the fieldwork indicated that sedimentation, the common diagnostic method for fascioliasis and schistosomiasis in livestock, was misclassifying schistosomiasis cases (false negatives). Consequently, the sensitivity of sedimentation for schistosomiasis diagnosis in cattle was tested and shown to be somewhat low due to eggs hatching during the sedimentation process, although sensitivity can be increased by adjusting the protocol in ways that inhibit egg hatching.
Schistosomiasis and fascioliasis have a high cost to society in terms of human morbidity and economic losses to farmers, especially in low-resource setting. They are complex problems that are influenced by biological and environmental factors, but also social factors such as politics, culture, economics and determinants of health. Further research is needed in West Africa, and specifically in Côte d’Ivoire, to ascertain the extent to which schistosomiasis and fascioliasis in livestock, and other definitive hosts, pose a risk to human health and NTD control and prevention goals. Human and animal health are intricately linked, especially in low-resources settings with sustenance farming. An integrated One Health approach is essential to tackle the complexity of NTDs and the SDGs if progress towards these goals is to be made.