Microsatellite Investigations of Multiple Echinococcus Granulosus Sensu Stricto Cysts in Single Hosts Reveal Different Patterns of Infection Events between Livestock and Humans.

Selim M’Rad,Gérald Umhang,Laure Bournez,Vanessa Bastid,Sana Mosbahi,Myriam Oudni-M’Rad,Franck Boué,Abdelallatif Nouri,Frédéric Grenouillet,Hamouda Babba

doi:10.3390/pathogens9060444

Abstract

Cystic echinococcosis (CE) caused by the cestode Echinococcus granulosus sensu lato (s.l.) is a worldwide zoonosis and E. granulosus 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 E. granulosus 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.

Highlights

Cystic echinococcosis (CE), previously known as hydatidosis, caused by the cestode Echinococcus granulosus sensu lato (s.l.) is a worldwide zoonosis
Spontaneous or trauma-induced primary cyst rupture leading to spillage of protoscoleces and/or parasitic stem cells may lead to the development of new cysts in the same organ, or at another site in the body [36]
Two cysts with the same microsatellite profile may result from two different infection events, and the probability of the occurrence of such events depends on the genetic diversity of E. granulosus s.s. in a given area

Summary

Introduction

Cystic echinococcosis (CE), previously known as hydatidosis, caused by the cestode Echinococcus granulosus sensu lato (s.l.) is a worldwide zoonosis. CE is frequently encountered in countries where pastoral livestock breeding is well developed [1]. 12.6/100,000 inhabitants, Tunisia is considered the most endemic Mediterranean area [2]. Mediterranean countries such as France or Italy, the SI is much lower and averages 0.42/100,000 and 1.6/100,000 inhabitants, respectively [3,4,5]. Human and herbivore infections are acquired through the oral ingestion of E. granulosus s.l eggs via vegetables and water, or for humans by direct contact with dogs [6]. Each viable oncosphere has the potential to develop into one CE cyst (larval stage), which is most commonly located in the liver and/or the lungs even though almost any organ may be affected [7]

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