Natural Intra- and Interclade Human Hybrid Schistosomes in Africa with Considerations on Prevention through Vaccination

Abstract

Causal agents of schistosomiasis are dioecious, digenean schistosomes affecting mankind in 76 countries. Preventive measures are manifold but need to be complemented by vaccination for long-term protection; vaccine candidates in advanced pre-clinical/clinical stages include Sm14, Sm-TSP-2/Sm-TSP-2Al®, Smp80/SchistoShield®, and Sh28GST/Bilhvax®. Natural and anthropogenic changes impact on breaking species isolation barriers favoring introgressive hybridization, i.e., allelic exchange among gene pools of sympatric, interbreeding species leading to instant large genetic diversity. Phylogenetic distance matters, thus the less species differ phylogenetically the more likely they hybridize. PubMed and Embase databases were searched for publications limited to hybridale confirmation by mitochondrial cytochrome c oxidase (COX) and/or nuclear ribosomal internal transcribed spacer (ITS). Human schistosomal hybrids are predominantly reported from West Africa with clustering in the Senegal River Basin, and scattering to Europe, Central and Eastern Africa. Noteworthy is the dominance of Schistosoma haematobium interbreeding with human and veterinary species leading due to hybrid vigor to extinction and homogenization as seen for S. guineensis in Cameroon and S. haematobium in Niger, respectively. Heterosis seems to advantage S. haematobium/S. bovis interbreeds with dominant S. haematobium-ITS/S. bovis-COX1 profile to spread from West to East Africa and reoccur in France. S. haematobium/S. mansoni interactions seen among Senegalese and Côte d’Ivoirian children are unexpected due to their high phylogenetic distance. Detecting pure S. bovis and S. bovis/S. curassoni crosses capable of infecting humans observed in Corsica and Côte d’Ivoire, and Niger, respectively, is worrisome. Taken together, species hybridization urges control and preventive measures targeting human and veterinary sectors in line with the One-Health concept to be complemented by vaccination protecting against transmission, infection, and disease recurrence. Functional and structural diversity of naturally occurring human schistosomal hybrids may impact current vaccine candidates requiring further research including natural history studies in endemic areas targeted for clinical trials.

Hybridization increases genetic diversity in Schistosoma haematobium populations infecting humans in Cameroon

“…Several studies have already been conducted on S. haematobium × S. bovis hybrids. They have been identified from samples collected from school-aged children in Niger [ 14 ], Senegal [ 13 , 15 – 19 ], Benin [ 20 , 21 ], Mali [ 22 ], Côte d'Ivoire [ 23 ], Malawi [ 24 ] and France [ 20 , 25 , 26 ]. The biological, epidemiological and pathological consequences of this hybridization are still unknown and warrant further investigation due to the potential risk of zoonotic transmission because the infection reservoirs have a significant impact on transmission and therefore on the elimination programme for these worms.…”

Clinical Applications of Isothermal Diagnosis for Human Schistosomiasis

“…The species S. mekongi, S. guineensis, S. intercalatum, and S. malayensis also affect humans, but to a lower extent [1,2]. Of growing concern is cross-species hybridization abated by natural and anthropogenic changes; it leads to a large diversity of novel inter-species and/or inter-lineages through instant acquisition of genetic information [3].…”

Mating Interactions between Schistosoma bovis and S. mansoni and Compatibility of Their F1 Progeny with Biomphalaria glabrata and Bulinus truncatus

“…These species belong to two different evolutionary lineages of schistosomes; the S. mansoni and the S. haematobium groups, respectively. S. mansoni is known to infect Humans, Non-Human Primates or rodents, while S. bovis is known to infect livestock and rodents [6]. In the field, both parasite species can share the same rodent host, as has been found in Mastomys huberti and Arvicanthis niloticus in Senegal [23].…”

“…Human schistosomiasis affects about 250 million people in about 78 countries worldwide, with the largest disease burden throughout sub-Saharan Africa [5]. The Schistosoma genus is composed of about 23 recognized species with at least 19 species that infect livestock and wild animals [6]. Although only five species are of veterinary importance to domestic animals, at least six species infect humans and are of medical interest [6].…”

“…The Schistosoma genus is composed of about 23 recognized species with at least 19 species that infect livestock and wild animals [6]. Although only five species are of veterinary importance to domestic animals, at least six species infect humans and are of medical interest [6]. Because several of these species are co-endemic and can share the same definitive host, interspecific crossing opportunities may occur.…”