Joséphine Foata

Outbreak of urogenital schistosomiasis in Corsica (France): an epidemiological case study

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.

Ultrastructural study of the spermatozoon of Nicolla testiobliquum (Digenea, Opecoelidae) parasite of brown trout Salmo trutta (Pisces, Teleostei)

The present paper describes the spermatozoon of Nicolla testiobliquum (Digenea, Opecoelidae), an intestinal parasite of brown trout Salmo trutta, studied by transmission electron microscopy. The mature spermatozoon possess two axonemes of 9 + “1” pattern, two mitochondria, a nucleus, external ornamentation of the plasma membrane, spine-like bodies and cortical microtubules. A comparative study between N. testiobliquum and Nicolla wisniewskii shows mainly two different dispositions of the two mitochondria in these two species of a same genera. Moreover, the comparison of each of these spermatozoon features with others digeneans, in general, and other Opecoelidae in particular, is also presented. It appears that the organisation of the posterior part of the spermatozoon, the disposition of cortical microtubules and external ornamentation associated with spine-like bodies could be interesting elements for phylogeny.

SPERMIOGENESIS AND SPERMATOZOON ULTRASTRUCTURE OF NICOLLA WISNIEWSKII (DIGENEA: OPECOELIDAE), AN INTESTINAL PARASITE OF BROWN TROUT SALMO TRUTTA (PISCES: TELEOSTEI)

Spermiogenesis and ultrastructure of spermatozoon of Nicolla wisniewskii (Digenea, Opecoelidae), an intestinal parasite of Salmo trutta, were studied by electron microscopy. Spermiogenesis follows the general pattern found in the Digenea. It begins with the formation of a differentiation zone, including striated rootlets associated with 2 centrioles and an intercentriolar body. The flagella undergo a rotation of greater than 90°. Then, their fusion with the median cytoplasmic process is proximodistal and asynchronous. A peculiarity was observed before the fusion of flagella, i.e., the attachment zones joined as 2 pairs by an electron-dense bridge. The mature spermatozoon is characterized by 2 axonemes, cortical microtubules, a nucleus, 2 mitochondria, external ornamentation, and spinelike bodies. At the posterior end of flagella, the spermatozoon is also characterized by the presence of a central element of the axoneme and without the 9 microtubule doublets. These results were compared with those of the other digeneans and, in particular, with other species of Opecoelidae. It appears that the number of cortical microtubules and their localization in the spermatozoon may be an interesting feature of their phylogeny.

Ultrastructural study of the spermatozoon of Pronoprymna ventricosa (Digenea, Baccigerinae), parasite of the twaite shad Alosa fallax Lacepede (Pisces, Teleostei)

In this paper, we describe the ultrastructural organisation of the spermatozoon of a Digenea Baccigerinae Pronoprymna ventricosa. This spermatozoon possesses the elements found in the others digeneans: two axonemes with 9 + “1” pattern, a mitochondrion, a nucleus, cortical microtubules and external ornamentations. However, this spermatozoon presents two particularities. The first is the presence of a single field of cortical microtubules disposed in the ventral side (mitochondrion side) of the spermatozoon. In the other digeneans, two fields of cortical microtubules are observed between the two axonemes. The second is the presence of external ornamentations not associated with cortical microtubules. These two points have, to our knowledge, never been described in another digenean. Moreover, a separation in two groups of the digenean spermatozoa is proposed in relation to the localisation of the external ornamentations. We propose to distinguish a first group exhibiting these elements in the proximal part of the spermatozoon and a second one with external ornamentations in a second part of the gamete.

Spermiogenesis and sperm ultrastructure of Deropristis Inflata Molin, 1859 (Digenea, Deropristidae), a parasite of Anguilla anguilla

To our knowledge, this paper describes the first ultrastructural results on spermiogenesis and the spermatozoon of a Digenea belonging to the family Deropristidae, Deropristis inflata. Spermiogenesis follows the usual pattern found in the digeneans, but a single noteworthy characteristic concerns the centriole, which presents a “prominent pear-shaped electron-dense region.” Spermiogenesis in D. inflata begins with the formation of a differentiation zone. The two centrioles give rise to flagella. These two flagella undergo a rotation of 90° and fuse with the median cytoplasmic process. The proximo-distal fusion occurs at the level of attachment zones. The mature spermatozoon of D. inflata possesses five regions and presents all the features found in the digenean gamete. However, several characteristics allow us to distinguish the spermatozoon of D. inflata from other digenetic trematoda, namely the external ornamentations of the plasmic membrane, the anterior and posterior extremities. Furthermore, the distal part of the nucleus in front of those of the mitochondria appears such a distinctive criterion in the spermatozoon of this species. Our ultrastructural investigations produce new data on the reproduction of D. inflata, which may be useful for the understanding of the phylogenetic relationships in the Deropristidae family.

ULTRASTRUCTURAL STUDY OF SPERMIOGENESIS AND THE SPERMATOZOON OF CREPIDOSTOMUM METOECUS (DIGENEA: ALLOCREADIIDAE), A PARASITE OF SALMO TRUTTA (PISCES: TELEOSTEI)

Spermiogenesis and the spermatozoon of Crepidostomum metoecus, an intestinal parasite of brown trout Salmo trutta, were studied by transmission electron microscopy. Spermiogenesis begins with the formation of a differentiation zone in front of 2 centrioles associated by an intercentriolar body. Each centriole is linked to a striated rootlet, and gives rise to a flagellum. The rotation of flagella is greater than 90°; their fusion with the median cytoplasmic extension is proximodistal and asynchronous. The spermatozoon is formed after constriction of arched membranes. The spermatozoon possesses 2 axonemes of the 9 + “1” pattern, a nucleus, mitochondria, and glycogen. A major feature is the presence, in the anterior part, of external ornamentation and a lateral expansion associated with spinelike bodies. Another attribute is the presence of 2 mitochondria rather than just 1, as in most of the digenean spermatozoa. To our knowledge, this study is the first undertaken with a species of the Allocreadiidae.

Spermatozoon Ultrastructure of Gyliauchen sp. (Digenea: Gyliauchenidae), an Intestinal Parasite of Siganus fuscescens (Pisces: Teleostei)

The ultrastructure of the mature spermatozoon of Gyliauchen sp., a parasite of the dusky rabbitfish Siganus fuscescens, was studied by transmission electron microscopy. The spermatozoon possesses two axonemes of the 9+“1” pattern of Trepaxonemata, four attachment zones, one mitochondrion, a nucleus, cortical microtubules, external ornamentation of the plasma membrane, and spine-like bodies. The main characteristics of this spermatozoon are the presence of one mitochondrion, spine-like bodies not associated with the external ornamentation, and a posterior extremity of type 3 that is characterized by the following sequence: posterior extremity of the nucleus then posterior extremity of the second axoneme. Numerous other ultrastructural features are also discussed and compared to the digenean spermatology literature. This is the first study of a member of the Gyliauchenidae and the fourth within the Lepocreadioidea. The results show that many ultrastructural characters are variable within this superfamily and could be useful for phylogeny.

Sperm ultrastructure of the digenean Siphoderina elongata (Platyhelminthes, Cryptogonimidae) intestinal parasite of Nemipterus furcosus (Pisces, Teleostei)

The ultrastructure of the spermatozoon of Siphoderina elongata was studied by transmission electron microscopy. A description and drawings of the mature spermatozoon are presented in this paper. Several ultrastructural elements of this male gamete have been observed: a nucleus, two mitochondria, two axonemes of 9 + “1” pattern, external ornamentation of the plasma membrane, spine-like bodies and cortical microtubules. The presence, the location or the number of these elements have been compared with other digenean spermatozoa. Moreover, a close attention was paid to the organization of the external ornamentation region. This zone presents a single row of cortical microtubules disposed in a semi-circle around a mitochondrion and associated with external ornamentation and spine-like bodies. The aim of this study is to highlight criteria which can be interesting in Platyhelminthes phylogeny.

Influence of season and host age on wild boar parasites in Corsica using indicator species analysis.

The indicator value (Ind Val) method which combines measures of fidelity and specificity has been used in a study on wild boar parasites in Corsica during 2001-2003. Because of its resilience to changes in abundance, IndVal is a particularly effective tool for ecological bioindication. The Ind Val method showed how season can influence the occurrence of parasite species in the wild boar, and also identified parasites as bioindicators relative to host age. The randomization test identified five parasite species having a significant indicator value for the season (the ticks, Hyalomma aegyptium and Rhipicephalus sanguineus, the louse, Haematopinus suis and the nematodes Globocephalus urosubulatus and Ascaris suum and two indicator species of an age class (the nematodes G. urosubulatus and Metastrongylus sp.). Data on species composition and infection levels would help improve the monitoring and management of parasitism in Suidae populations.

Topography and Ultrastructure of the Tegument of Bucephalus anguillae (Digenea: Bucephalidae), a Parasite of the European Eel Anguilla anguilla (Osteichthyen: Anguillidae)

Abstract The tegumental ultrastructure of the intestinal fluke Bucephalus anguillae was studied with the use of scanning and transmission electron microscopy. The surface of the tegument is covered by transverse ridges from which protrude numerous closely packed, digitated, and claw-shaped spines. Cobblestone-like units of the tegument were observed on the crescent-shaped formation of the rhynchus and at the posterior part of the body. Three types of sensory structures were examined, i.e., 2 uniciliated receptors and 1 without cilia. As anterior–posterior differences were observed, particular attention was given to spines and sensory receptors. Spine insertion zones and average cilia length are variable between anterior and posterior tegument areas. Ultrastructural study revealed that the tegument of B. anguillae has a typical syncytial organization with a distal cytoplasm lying over a basal matrix and cytons below. Cytoplasmic bridges allowed transit of secretory vesicles and granules. Diagrams of spines and sensory receptors were made to help in understanding the nature of these structures.