Children of Senegal River Basin show the highest prevalence of Blastocystis sp. ever observed worldwide

Dima El Safadi 0 2 3 Lobna Gaayeb 0 1 3 Dionigia Meloni 0 3 5 Amandine Cian 0 3 Philippe Poirier 4 Ivan Wawrzyniak 4 Frdric Delbac 4 Fouad Dabboussi 2 Laurence Delhaes 0 3 Modou Seck 1 Monzer Hamze 2 Gilles Riveau 0 1 3 Eric Viscogliosi 0 3 0 Institut Pasteur de Lille, Centre d'Infection et d'Immunite de Lille (CIIL), Inserm U1019, CNRS UMR 8204, Universite Lille Nord de France , 1 rue du Professeur Calmette, BP 245, 59019 Lille cedex , France 1 Biomedical Research Center Espoir pour la Sante (CRB-EPLS) , Saint-Louis , Senegal 2 Centre AZM pour la Recherche en Biotechnologie et ses Applications, Laboratoire Microbiologie, Sante et Environnement, Universite Libanaise , Tripoli , Lebanon 3 Institut Pasteur de Lille, Centre d'Infection et d'Immunite de Lille (CIIL), Inserm U1019, CNRS UMR 8204, Universite Lille Nord de France , 1 rue du Professeur Calmette, BP 245, 59019 Lille cedex , France 4 Laboratoire Microorganismes: Genome et Environnement, CNRS UMR 6023, Universite Blaise Pascal de Clermont-Ferrand , Aubiere , France 5 Microbe Division/Japan Collection of Microorganisms (JCM), RIKEN BioResource Center , Tsukuba , Japan Background: Blastocystis sp. is currently the most common intestinal protist found in human feces and considered an emerging parasite with a worldwide distribution. Because of its potential impact in public health, we reinforced the picture of Blastocystis sp. prevalence and molecular subtype distribution in Africa by performing the first survey of this parasite in Senegal. Methods: Stool samples from 93 symptomatic presenting with various gastrointestinal disorders or asymptomatic children living in three villages of the Senegal River Basin were tested for the presence of Blastocystis sp. by nonquantitative and quantitative PCR using primer pairs targeting the SSU rDNA gene. Positive samples were subtyped to investigate the frequency of Blastocystis sp. subtypes in our cohort and the distribution of subtypes in the symptomatic and asymptomatic groups of children. Results: By the use of molecular tools, all 93 samples were found to be positive for Blastocystis sp. indicating a striking parasite prevalence of 100%. Mixed infections by two or three subtypes were identified in eight individuals. Among a total of 103 subtyped isolates, subtype 3 was most abundant (49.5%) followed by subtype 1 (28.2%), subtype 2 (20.4%) and subtype 4 (1.9%). Subtype 3 was dominant in the symptomatic group while subtypes 1 and 2 were detected with equal frequency in both symptomatic and asymptomatic groups. The distribution of subtypes was compared with those available in other African countries and worldwide. Comparison confirmed that subtype 4 is much less frequently detected or absent in Africa while it is commonly found in Europe. Potential sources of Blastocystis sp. infection including human-to-human, zoonotic, and waterborne transmissions were also discussed. Conclusions: The prevalence of Blastocystis sp. in our Senegalese population was the highest prevalence ever recovered worldwide for this parasite by reaching 100%. All cases were caused by subtypes 1, 2, 3 and 4 with a predominance of subtype 3. More than half of the children infected by Blastocystis sp. presented various gastrointestinal disorders. Such high prevalence of blastocystosis in developing countries makes its control a real challenge for public health authorities. - Background Blastocystis sp. is an anaerobic protist that inhabits the gastrointestinal tract of humans and many groups of animals [1-4]. This cosmopolitan enteric parasite with a worldwide distribution [5] is often identified as the most common unicellular eukaryote reported in human fecal samples [1]. Indeed, its prevalence may exceed 50% in developing countries [6,7] and reach 20% in industrialized countries [8,9]. These differences may be explained by poor sanitary conditions, close animal contact, and consumption of contaminated food or water [10-12]. Such prevalence also suggests large-scale human-tohuman [13], waterborne, and zoonotic transmissions for Blastocystis sp. [14]. Numerous studies have demonstrated the resistance of cysts of the parasite in feces and environmental sources [15] highlighting the fecal-oral route as the main mode of transmission of Blastocystis sp. Moreover, a higher risk of infection has been identified in food and animal handlers, providing conclusive evidence on the transmission of the parasite between humans and animals [16,17]. At the morphological level, Blastocystis sp. isolates from humans and animals have been reported to be roughly indistinguishable [1]. However, extensive genetic diversity among Blastocystis sp. isolates has been reported based on the comparison of the small-subunit (SSU) rDNA gene sequence [18] leading to the classification of Blastocystis sp. isolates into subtypes (STs) [19]. To date, according to recent epidemiological surveys in human and animal populations, 17 STs have been identified [2] but it is highly likely that other STs remain yet to be uncovered. Among the 17 STs, nine of them have been detected in humans with a varying prevalence [5]. Indeed, only four of them are frequent (ST1, ST2, ST3 and ST4) and represent around 90% of the subtyped isolates. A majority of human infections with Blastocystis sp. is attributable to ST3 but the distribution of the four predominant STs may vary among the areas studied. Thereby, ST4 is almost as common as ST1 and ST3 in some European countries but seems rare or completely absent in Africa, Asia, and America [5,20]. The other STs that are common in animal hosts i.e. ST5 to ST9, are rarely found in humans and are most likely the result of zoonotic transmission. As Blastocystis sp. can be found in both symptomatic and asymptomatic patients its clinical relevance remained uncertain [1]. However, a converging bundle of recent in vivo, in vitro and genomic data strongly suggests that this microorganism may be pathogen [21-24] and allows proposing a model for pathogenesis of this parasite [25] particularly involving virulence factors as cysteine proteases [26,27]. Therefore, Blastocystis sp. should be associated with a variety of non-specific gastrointestinal disorders including diarrhea, abdominal pain, nausea and vomiting [1,22] and also suspected to be linked to irritable bowel syndrome (IBS) [25,28] and chronic or acute urticarial lesions [29,30]. In addition, Blastocystis sp. has increasingly been implicated in diarrheal illness in immunocompromised individuals including HIV/AIDS and cancer patients and transplant recipients [31,32]. It has long been suggested that the pathogenesis of Blastocystis sp. may be dependent upon ST but recent epidemiological data remain contradictory [8,29,33-36]. Nevertheless, the likely pathogenic power of Blastocystis sp. coupled to its high prevalence in the human population raise crucial questions about its current burden in public health. Consequently, information on the prevalence of the p (...truncated)