Microsatellite Investigations of Multiple <i>Echinococcus granulosus</i> Sensu Stricto Cysts in Single Hosts Reveal Different Patterns of Infection Events between Livestock and Humans

Cystic echinococcosis (CE) caused by the cestode <i>Echinococcus granulosus</i> sensu lato (s.l.) is a worldwide zoonosis and <i>E. granulosus</i> sensu stricto (s.s.) is the most common species associated with animal and human diseases. The objective of this study was to obt...

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Main Authors: Selim M’rad, Myriam Oudni-M’rad, Vanessa Bastid, Laure Bournez, Sana Mosbahi, Abdelallatif Nouri, Hamouda Babba, Frédéric Grenouillet, Franck Boué, Gérald Umhang
Format: Article
Language:English
Published: MDPI AG 2020-06-01
Series:Pathogens
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Online Access:https://www.mdpi.com/2076-0817/9/6/444
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author Selim M’rad
Myriam Oudni-M’rad
Vanessa Bastid
Laure Bournez
Sana Mosbahi
Abdelallatif Nouri
Hamouda Babba
Frédéric Grenouillet
Franck Boué
Gérald Umhang
author_facet Selim M’rad
Myriam Oudni-M’rad
Vanessa Bastid
Laure Bournez
Sana Mosbahi
Abdelallatif Nouri
Hamouda Babba
Frédéric Grenouillet
Franck Boué
Gérald Umhang
author_sort Selim M’rad
collection DOAJ
description Cystic echinococcosis (CE) caused by the cestode <i>Echinococcus granulosus</i> sensu lato (s.l.) is a worldwide zoonosis and <i>E. granulosus</i> sensu stricto (s.s.) is the most common species associated with animal and human diseases. The objective of this study was to obtain a better understanding of CE infection in livestock and humans from very low and high endemic areas—France and Tunisia—by studying the genetic diversity of <i>E. granulosus</i> s.s. at the intra-individual host level. This genetic diversity was studied using EgSca6 and EgSca11 microsatellite profiles in 93 sheep from France and Tunisia, and in 12 cattle and 31 children from Tunisia only, all presenting multiple CE cysts (2 to 10 cysts). Overall, 96% of sheep, 92% of cattle, and 48% of children had at least two cysts with different microsatellite profiles. Inversely, 35% of sheep, 17% of cattle, and 65% of children had at least two cysts with the same microsatellite profile. The genotyping results for the CE samples highlight high and similar genetic diversity in France and Tunisia, suggesting that the probability of being successively infected by CE of the same microsatellite profile was rare in both countries. Therefore, our results suggest that in rare cases, several eggs of the same microsatellite profile, from two to seven in our data, can be ingested simultaneously in a single infection event and develop into several cysts in livestock and children. They also indicate that multiple infection events are frequent in livestock, even in a low endemic country such as France, and are less frequent but not negligible in children in a high endemic country such as Tunisia. Moreover, this is the first time that genetic evidence of secondary CE has been found. Further studies are needed to better assess the pattern of infection events in livestock and humans, especially by studying the genetic diversity of adult worms in definitive hosts.
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spelling doaj.art-ec0675e967cd439b89ce7a3e606acfe32023-11-20T02:55:44ZengMDPI AGPathogens2076-08172020-06-019644410.3390/pathogens9060444Microsatellite Investigations of Multiple <i>Echinococcus granulosus</i> Sensu Stricto Cysts in Single Hosts Reveal Different Patterns of Infection Events between Livestock and HumansSelim M’rad0Myriam Oudni-M’rad1Vanessa Bastid2Laure Bournez3Sana Mosbahi4Abdelallatif Nouri5Hamouda Babba6Frédéric Grenouillet7Franck Boué8Gérald Umhang9Laboratory of Medical and Molecular Parasitology-Mycology (LP3M), LR12ES08, Faculty of Pharmacy, University of Monastir, Monastir 5000, TunisiaLaboratory of Medical and Molecular Parasitology-Mycology (LP3M), LR12ES08, Faculty of Pharmacy, University of Monastir, Monastir 5000, TunisiaAnses LRFSN, Wildlife Surveillance and Eco-Epidemiology Unit, National Reference Laboratory for <i>Echinococcus</i> spp., 54220 Malzéville, FranceAnses LRFSN, Wildlife Surveillance and Eco-Epidemiology Unit, National Reference Laboratory for <i>Echinococcus</i> spp., 54220 Malzéville, FrancePaediatric Surgery Department, F. Bourguiba Hospital, Monastir, Medical School, Monastir 5000, TunisiaPaediatric Surgery Department, F. Bourguiba Hospital, Monastir, Medical School, Monastir 5000, TunisiaLaboratory of Medical and Molecular Parasitology-Mycology (LP3M), LR12ES08, Faculty of Pharmacy, University of Monastir, Monastir 5000, TunisiaChrono-Environnement UMR 6249 Research Team, CNRS-University of Bourgogne-Franche-Comté, 25030 Besançon, FranceAnses LRFSN, Wildlife Surveillance and Eco-Epidemiology Unit, National Reference Laboratory for <i>Echinococcus</i> spp., 54220 Malzéville, FranceAnses LRFSN, Wildlife Surveillance and Eco-Epidemiology Unit, National Reference Laboratory for <i>Echinococcus</i> spp., 54220 Malzéville, FranceCystic echinococcosis (CE) caused by the cestode <i>Echinococcus granulosus</i> sensu lato (s.l.) is a worldwide zoonosis and <i>E. granulosus</i> sensu stricto (s.s.) is the most common species associated with animal and human diseases. The objective of this study was to obtain a better understanding of CE infection in livestock and humans from very low and high endemic areas—France and Tunisia—by studying the genetic diversity of <i>E. granulosus</i> s.s. at the intra-individual host level. This genetic diversity was studied using EgSca6 and EgSca11 microsatellite profiles in 93 sheep from France and Tunisia, and in 12 cattle and 31 children from Tunisia only, all presenting multiple CE cysts (2 to 10 cysts). Overall, 96% of sheep, 92% of cattle, and 48% of children had at least two cysts with different microsatellite profiles. Inversely, 35% of sheep, 17% of cattle, and 65% of children had at least two cysts with the same microsatellite profile. The genotyping results for the CE samples highlight high and similar genetic diversity in France and Tunisia, suggesting that the probability of being successively infected by CE of the same microsatellite profile was rare in both countries. Therefore, our results suggest that in rare cases, several eggs of the same microsatellite profile, from two to seven in our data, can be ingested simultaneously in a single infection event and develop into several cysts in livestock and children. They also indicate that multiple infection events are frequent in livestock, even in a low endemic country such as France, and are less frequent but not negligible in children in a high endemic country such as Tunisia. Moreover, this is the first time that genetic evidence of secondary CE has been found. Further studies are needed to better assess the pattern of infection events in livestock and humans, especially by studying the genetic diversity of adult worms in definitive hosts.https://www.mdpi.com/2076-0817/9/6/444cystic echinococcosis<i>Echinococcus granulosus</i> sensu strictomicrosatelliteintra-individual genetic diversityinfection eventrecurrence
spellingShingle Selim M’rad
Myriam Oudni-M’rad
Vanessa Bastid
Laure Bournez
Sana Mosbahi
Abdelallatif Nouri
Hamouda Babba
Frédéric Grenouillet
Franck Boué
Gérald Umhang
Microsatellite Investigations of Multiple <i>Echinococcus granulosus</i> Sensu Stricto Cysts in Single Hosts Reveal Different Patterns of Infection Events between Livestock and Humans
Pathogens
cystic echinococcosis
<i>Echinococcus granulosus</i> sensu stricto
microsatellite
intra-individual genetic diversity
infection event
recurrence
title Microsatellite Investigations of Multiple <i>Echinococcus granulosus</i> Sensu Stricto Cysts in Single Hosts Reveal Different Patterns of Infection Events between Livestock and Humans
title_full Microsatellite Investigations of Multiple <i>Echinococcus granulosus</i> Sensu Stricto Cysts in Single Hosts Reveal Different Patterns of Infection Events between Livestock and Humans
title_fullStr Microsatellite Investigations of Multiple <i>Echinococcus granulosus</i> Sensu Stricto Cysts in Single Hosts Reveal Different Patterns of Infection Events between Livestock and Humans
title_full_unstemmed Microsatellite Investigations of Multiple <i>Echinococcus granulosus</i> Sensu Stricto Cysts in Single Hosts Reveal Different Patterns of Infection Events between Livestock and Humans
title_short Microsatellite Investigations of Multiple <i>Echinococcus granulosus</i> Sensu Stricto Cysts in Single Hosts Reveal Different Patterns of Infection Events between Livestock and Humans
title_sort microsatellite investigations of multiple i echinococcus granulosus i sensu stricto cysts in single hosts reveal different patterns of infection events between livestock and humans
topic cystic echinococcosis
<i>Echinococcus granulosus</i> sensu stricto
microsatellite
intra-individual genetic diversity
infection event
recurrence
url https://www.mdpi.com/2076-0817/9/6/444
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