Jérôme Boissier1, Sébastien Grech-Angelini2, Bonnie L Webster3, Jean-François Allienne4, Tine Huyse5, Santiago Mas-Coma6, Eve Toulza4, Hélène Barré-Cardi7, David Rollinson3, Julien Kincaid-Smith4, Ana Oleaga8, Richard Galinier4, Joséphine Foata9, Anne Rognon4, Antoine Berry10, Gabriel Mouahid4, Rémy Henneron11, Hélène Moné4, Harold Noel12, Guillaume Mitta4. 1. Université de Perpignan Via Domitia, IHPE UMR 5244, CNRS, IFREMER, Université de Montpellier, Perpignan, France. Electronic address: boissier@univ-perp.fr. 2. INRA, Laboratoire de recherches sur le développement de l'élevage, Corte, France. 3. Department of Life Sciences, Parasites and Vectors Division, Natural History Museum, London, UK; London Centre for Neglected Tropical Disease Research, London, UK. 4. Université de Perpignan Via Domitia, IHPE UMR 5244, CNRS, IFREMER, Université de Montpellier, Perpignan, France. 5. Department of Biology, Royal Museum for Central Africa, Tervuren, Belgium; Laboratory of Biodiversity and Evolutionary Genomics, Biology, University of Leuven, Leuven, Belgium. 6. Departamento de Parasitologia, Facultad de Farmacia, Universidad de Valencia, Burjassot, Valencia, Spain. 7. OCIC, ECOTER, Office de l'Environnement de la Corse, Corte, France; Unité de suivi entomologique et de politique de lutte anti vectorielle, Agence régionale de santé de Corse, Ajaccio, France. 8. Parasitology Laboratory, Instituto de Recursos Naturales y Agrobiología de Salamanca (IRNASA, CSIC), Salamanca, Spain. 9. Equipe parasites et écosystèmes méditerranéens, UMR 6134 CNRS SPE Science pour l'environnement, Université de Corse Pascal Paoli, Corte, France. 10. Service de Parasitologie-Mycologie, CHU Toulouse and Centre de Physiopathologie de Toulouse Purpan, INSERM U1043, CNRS UMR5282, Université de Toulouse, Toulouse, France. 11. Hôpital Sainte Marguerite, Hopitaux Sud de Marseille, Marseille, France. 12. French Institute for Public Health Surveillance (Institut de Veille Sanitaire, InVS), Saint-Maurice, France.
Abstract
BACKGROUND: Schistosomiasis is a snail-borne parasitic disease endemic in several tropical and subtropical countries. However, in the summer of 2013, an unexpected outbreak of urogenital schistosomiasis occurred in Corsica, with more than 120 local people or tourists infected. We used a multidisciplinary approach to investigate the epidemiology of urogenital schistosomiasis in Corsica, aiming to elucidate the origin of the outbreak. METHODS: We did parasitological and malacological surveys at nine potential sites of infection. With the snails found, we carried out snail-parasite compatibility experiments by exposing snails to schistosome larvae recovered from the urine of a locally infected Corsican patient. Genetic analysis of both mitochondrial (cox1) and nuclear (internal transcribed spacer) DNA data from the Schistosoma eggs or miracidia recovered from the infected patients was conducted to elucidate the epidemiology of this outbreak. FINDINGS: We identified two main infection foci along the Cavu River, with many Bulinus truncatus snails found in both locations. Of the 3544 snails recovered across all sites, none were naturally infected, but laboratory-based experimental infections confirmed their compatibility with the schistosomes isolated from patients. Molecular characterisation of 73 eggs or miracidia isolated from 12 patients showed infection with Schistosoma haematobium, S haematobium-Schistosoma bovis hybrids, and S bovis. Further sequence data analysis also showed that the Corsican schistosomes were closely related to those from Senegal in west Africa. INTERPRETATION: The freshwater swimming pools of the Cavu River harbour many B truncatus snails, which are capable of transmitting S haematobium-group schistosomes. Our molecular data suggest that the parasites were imported into Corsica by individuals infected in west Africa, specifically Senegal. Hybridisation between S haematobium and the cattle schistosome S bovis had a putative role in this outbreak, showing how easily and rapidly urogenital schistosomiasis can be introduced and spread into novel areas where Bulinus snails are endemic, and how hybridisation could increase the colonisation potential of schistosomes. Furthermore our results show the potential risk of schistosomiasis outbreaks in other European areas, warranting close monitoring and surveillance of all potential transmission foci. FUNDING: WHO, ANSES, RICET, and the Ministry of Health and Consumption.
BACKGROUND:Schistosomiasis is a snail-borne parasitic disease endemic in several tropical and subtropical countries. However, in the summer of 2013, an unexpected outbreak of urogenital schistosomiasis occurred in Corsica, with more than 120 local people or tourists infected. We used a multidisciplinary approach to investigate the epidemiology of urogenital schistosomiasis in Corsica, aiming to elucidate the origin of the outbreak. METHODS: We did parasitological and malacological surveys at nine potential sites of infection. With the snails found, we carried out snail-parasite compatibility experiments by exposing snails to schistosome larvae recovered from the urine of a locally infected Corsican patient. Genetic analysis of both mitochondrial (cox1) and nuclear (internal transcribed spacer) DNA data from the Schistosoma eggs or miracidia recovered from the infected patients was conducted to elucidate the epidemiology of this outbreak. FINDINGS: We identified two main infection foci along the Cavu River, with many Bulinus truncatus snails found in both locations. Of the 3544 snails recovered across all sites, none were naturally infected, but laboratory-based experimental infections confirmed their compatibility with the schistosomes isolated from patients. Molecular characterisation of 73 eggs or miracidia isolated from 12 patients showed infection with Schistosoma haematobium, S haematobium-Schistosoma bovis hybrids, and S bovis. Further sequence data analysis also showed that the Corsican schistosomes were closely related to those from Senegal in west Africa. INTERPRETATION: The freshwater swimming pools of the Cavu River harbour many B truncatus snails, which are capable of transmitting S haematobium-group schistosomes. Our molecular data suggest that the parasites were imported into Corsica by individuals infected in west Africa, specifically Senegal. Hybridisation between S haematobium and the cattle schistosome S bovis had a putative role in this outbreak, showing how easily and rapidly urogenital schistosomiasis can be introduced and spread into novel areas where Bulinus snails are endemic, and how hybridisation could increase the colonisation potential of schistosomes. Furthermore our results show the potential risk of schistosomiasis outbreaks in other European areas, warranting close monitoring and surveillance of all potential transmission foci. FUNDING: WHO, ANSES, RICET, and the Ministry of Health and Consumption.
Authors: Nerea Castillo-Fernández; Manuel J Soriano-Pérez; Ana B Lozano-Serrano; José C Sánchez-Sánchez; Antonio Villarejo-Ordóñez; José A Cuenca-Gómez; José Vázquez-Villegas; María I Cabeza-Barrera; Joaquín Salas-Coronas Journal: Infection Date: 2021-05-04 Impact factor: 3.553