Interactions between intermediate snail hosts of the genus Bulinus and schistosomes of the Schistosoma haematobium group.
TL;DR: Biological factors central to the transmission of schistosomes, including cercarial emergence rhythms and interactions with other parasites and abiotic factors including temperature, rainfall, water velocity, desiccation and salinity are shown to impact on the intermediate host-parasite relationship.
Abstract: Within each of the four species groups of Bulinus there are species that act as intermediate hosts for one or more of the seven species of schistosomes in the Schistosoma haematobium group, which includes the important human pathogens S. haematobium and S. intercalatum. Bulinus species have an extensive distribution throughout much of Africa and some surrounding islands including Madagascar, parts of the Middle East and the Mediterranean region. Considerable variation in intermediate host specificity can be found and differences in compatibility between snail and parasite can be observed over small geographical areas. Molecular studies for detection of genetic variation and the discrimination of Bulinus species are reviewed and two novel assays, allele-specific amplification (ASA) and SNaPshot™, are introduced and shown to be of value for detecting nucleotide changes in characterized genes such as cytochrome oxidase 1. The value and complexity of compatibility studies is illustrated by case studies of S. haematobium transmission. In Senegal, where B. globosus, B. umbilicatus, B. truncatus and B. senegalensis may act as intermediate hosts, distinct differences have been observed in the infectivity of different isolates of S. haematobium. In Zanzibar, molecular characterization studies to discriminate between B. globosus and B. nasutus have been essential to elucidate the roles of snails in transmission. B. globosus is an intermediate host on Unguja and Pemba. Further studies are required to establish the intermediate hosts in the coastal areas of East Africa. Biological factors central to the transmission of schistosomes, including cercarial emergence rhythms and interactions with other parasites and abiotic factors including temperature, rainfall, water velocity, desiccation and salinity are shown to impact on the intermediate host-parasite relationship.
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University of Montpellier1, Institut national de la recherche agronomique2, Natural History Museum3, Royal Museum for Central Africa4, Katholieke Universiteit Leuven5, University of Valencia6, Spanish National Research Council7, University of Corsica Pascal Paoli8, University of Toulouse9, Institut de veille sanitaire10
TL;DR: The molecular data suggest that the parasites were imported into Corsica by individuals infected in west Africa, specifically Senegal, and hybridisation between S haematobium and the cattle schistosome S bovis had a putative role in this outbreak.
Abstract: Summary 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.
207 citations
TL;DR: For all five countries, the information assembled in the current atlas provides the most reliable, up-to-date and comprehensive source of data on the distribution of common helminth infections to guide the rational implementation of control efforts.
Abstract: Reliable and updated maps of helminth (worm) infection distributions are essential to target control strategies to those populations in greatest need. Although many surveys have been conducted in endemic countries, the data are rarely available in a form that is accessible to policy makers and the managers of public health programmes. This is especially true in sub-Saharan Africa, where empirical data are seldom in the public domain. In an attempt to address the paucity of geographical information on helminth risk, this article describes the development of an updated global atlas of human helminth infection, showing the example of East Africa. Empirical, cross-sectional estimates of infection prevalence conducted since 1980 were identified using electronic and manual search strategies of published and unpublished sources. A number of inclusion criteria were imposed for identified information, which was extracted into a standardized database. Details of survey population, diagnostic methods, sample size and numbers infected with schistosomes and soil-transmitted helminths were recorded. A unique identifier linked each record to an electronic copy of the source document, in portable document format. An attempt was made to identify the geographical location of each record using standardized geolocation procedures and the assembled data were incorporated into a geographical information system. At the time of writing, over 2,748 prevalence surveys were identified through multiple search strategies. Of these, 2,612 were able to be geolocated and mapped. More than half (58%) of included surveys were from grey literature or unpublished sources, underlining the importance of reviewing in-country sources. 66% of all surveys were conducted since 2000. Comprehensive, countrywide data are available for Burundi, Rwanda and Uganda. In contrast, information for Kenya and Tanzania is typically clustered in specific regions of the country, with few records from areas with very low population density and/or environmental conditions which are unfavourable for helminth transmission. Information is presented on the prevalence and geographical distribution for the major helminth species. For all five countries, the information assembled in the current atlas provides the most reliable, up-to-date and comprehensive source of data on the distribution of common helminth infections to guide the rational implementation of control efforts.
161 citations
TL;DR: It is suggested that improved incorporation of transmission dynamics into spatial models and assessment of uncertainties inherent in data and modelling approaches represent important future research directions.
Abstract: This paper reviews recent studies on the spatial epidemiology of human schistosomiasis in Africa. The integrated use of geographical information systems, remote sensing and geostatistics has provided new insights into the ecology and epidemiology of schistosomiasis at a variety of spatial scales. Because large-scale patterns of transmission are influenced by climatic conditions, an increasing number of studies have used remotely sensed environmental data to predict spatial distributions, most recently using Bayesian methods of inference. Such data-driven approaches allow for a more rational implementation of intervention strategies across the continent. It is suggested that improved incorporation of transmission dynamics into spatial models and assessment of uncertainties inherent in data and modelling approaches represent important future research directions.
150 citations
Cites background from "Interactions between intermediate s..."
...Genetic differences in interspecific and intraspecific intermediate host–parasite interactions and infectivity may also play a role (Rollinson et al., 2001), although this aspect remains poorly understood....
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TL;DR: It is argued that greater research effort and focus are needed to improve understanding of this neglected tropical disease, and the inappropriateness of relying solely on data concerning the much more extensively studied intestinal form of schistosomiasis caused by S. haematobium is highlighted.
Abstract: This review considers the current status of urinary schistosomiasis, caused by infection with Schistosoma haematobium, and argues that greater research effort and focus are needed to improve understanding of this neglected tropical disease (NTD). The inappropriateness of relying solely on data concerning the much more extensively studied intestinal form of schistosomiasis caused by S. mansoni is highlighted. The current lack of genome and transcriptome information for S. haematobium is directly hindering further targeted research and must be quickly rectified. Recent molecular phylogenies caution the expectation of similarities between schistosome species and highlight the close relationships of species within the S. haematobium group. Treatment, current and prospective drugs and vaccines, together with diagnosis are considered, highlighting the differences associated with urinary schistosomiasis. This infection has a significant and specific impact on the urino-genital system and has a strong association with bladder cancer, leading to severe and chronic morbidity. There is a clear need for new clinical initiatives in this area to better quantify the disease burden. Furthermore, emerging associations with HIV and other pathogens need to be closely monitored. Research is urgently needed to improve current knowledge in order to develop the next generation of control tools.
134 citations
Cites background or methods from "Interactions between intermediate s..."
...…and compatibility, with both genetic and environmental factors playing a role in determining small-scale heterogeneities in schistosomiasis transmission, factors which need to be taken into account when focusing and improving schistosomiasis control at the local level (Rollinson et al. 2001)....
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...Rollinson et al. (2001) used 2 molecular assays, allele-specific amplification (ASA) and SNaPshot, in case studies in Senegal, where B. globosus, B. umbilicatus, B. truncatus and B. senegalensis may act as intermediate hosts for S. haematobium, and in Zanzibar to discriminate between B. globosus…...
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TL;DR: The study of the Planorbidae poses fundamental questions regarding how and when Schistosoma acquired new snail hosts, including how switches to relatively distant hosts are accomplished and why some available planorbids were not colonized.
Abstract: The Planorbidae represent one of the most important families of freshwater snails. They have a wide distribution and are significant both medically and economically as intermediate hosts for trematode worms. Digenetic trematodes of the genus Schistosoma cause schistosomiasis, a disease that infects 200 million people, and domestic animals throughout the tropics. Three of the four recognized species groups of Schistosoma rely on snails of the family Planorbidae to complete their life cycles. Each species group requires a specific planorbid genus-Bulinus, Biomphalaria, or Indoplanorbis. Our understanding of the relationships among the genera within the Planorbidae is rudimentary and based solely on internal anatomy and shell morphology. Two molecular markers, ribosomal 28S and actin exon 2, were sequenced and a phylogeny constructed for 38 taxa representing 16 planorbid genera. The phylogeny supports the division of the Planorbidae into two subfamilies, the Bulininae and Planorbinae. Interestingly, two representatives of the family Ancylidae fall within the Planorbidae highlighting the need for further analysis and possible reclassification of this group. A molecular based phylogeny of the genus Schistosoma was then mapped against the snail tree. The trees indicate that planorbid-transmitted Schistosoma appear not to be co-speciating with their current snail host lineages. Rather, host switching was prominent, including a switch involving two distantly related planorbid genera, Biomphalaria and Bulinus. Our study of the Planorbidae poses fundamental questions regarding how and when Schistosoma acquired new snail hosts, including how switches to relatively distant hosts are accomplished and why some available planorbids were not colonized.
113 citations
References
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Book•
01 Jan 1980
TL;DR: The biology of bulinus snail control local snail faunas chemical and physical factors life cycles and populations regions, lakes and rivers - biography.
Abstract: The first half of this book is primarily a systematic survey of the snails, beginning with glossaries, keys for identification to genera and a checklist of species. This is followed by a synopsis of species, with brief notes on ecology, distribution and parasites. Relationships are then described between snails and schistosomes and with other paras
1,076 citations
TL;DR: The degree of similarity of the banding patterns can be used to estimate nucleotide diversity and nucleotide divergence and the restrictions and criteria that must be met when RAPD data are used for estimating population genetic parameters are summarized.
Abstract: The technique of random amplification of polymorphic DNA (RAPD), which is simply polymerase chain reaction (PCR) amplification of genomic DNA by a single short oligonucleotide primer, produces complex patterns of anonymous polymorphic DNA fragments. The information provided by these banding patterns has proved to be of great utility for mapping and for verification of identity of bacterial strains. Here we consider whether the degree of similarity of the banding patterns can be used to estimate nucleotide diversity and nucleotide divergence. With haploid data, fragments generated by RAPD-PCR can be treated in a fashion very similar to that for restriction-fragment data. Amplification of diploid samples, on the other hand, requires consideration of the fact that presence of a band is dominant to absence of the band. After describing a method for estimating nucleotide divergence on the basis of diploid samples, we summarize the restrictions and criteria that must be met when RAPD data are used for estimating population genetic parameters.
310 citations
"Interactions between intermediate s..." refers background in this paper
...It was concluded that the nucleotide divergence within the genus went beyond the phylogenetic scope of the technique which is limited to samples of less than 10% divergence across actual or potential RAPD priming sites [see simulations of Clark & Lanigan (1993) and Stothard (1997)]....
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TL;DR: Cercariae, like miracidia, are non-parasitic larval stages implicated in the life cycle of all trematodes for the host-to-host parasite transmission.
Abstract: Cercariae, like miracidia, are non-parasitic larval stages implicated in the life cycle of all trematodes for the host-to-host parasite transmission. Almost all cercariae are free-living in the external environment. With a few exceptions (cercariae of Halipegus occidualis (Halipegidae) can live several months, Shostak & Esch, 1990a), cercariae have a short active life during which they do not feed, living on accumulated reserves. Most cercariae encyst as metacercariae in second intermediate hosts which are prey of the definitive host; in certain species, the interruption of the active life is achieved by an encystment in the external environment (or a simple immobile waiting strategy in a few species). In some two-host life cycles, the cercariae develop into adults after penetration (this is the case for various species causing human schistosomiasis). Some cercariae do not leave the mollusc which must then be ingested by the definitive host.
180 citations
"Interactions between intermediate s..." refers background in this paper
...Thus, cercarial rhythms may be considered as an adaptive behaviour increasing the probabilities of a meeting between parasite and host (Combes et al. 1994)....
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...…considerable interspecific diversity in cercarial emergence rhythms within the genus Schistosoma, with emergence peaks occurring at different times of the nycthemere (a 24 h photocycle), ranging between 08±00 and 09±00 h for the earliest, to 22±00 h and 23±00 h for the latest (Combes et al. 1994)....
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TL;DR: Attention is drawn to the need to make field observations at an appropriate spatial scale and also to the implications for the effectiveness of focal snail control as a means of reducing transmission.
Abstract: Populations of Bulinus globosus and Biomphalaria pfeifferi were studied in a river habitat in Zimbabwe over a period of 12 months. Data were obtained on the prevalences of infections of Schistosoma haematobium (also S. mattheei) and S. mansoni respectively. Population parameters showed the following patterns for both snail species. (1) A patchy distribution correlated with the distributions of aquatic plants. (2) Life-expectancies of only a few weeks. (3) Recruitment rates correlated with water temperature and showing a distinct seasonal peak. (4) Spatial variation in recruitment. (5) A redistribution of snails during the rainy season. Epidemiological parameters showed the following patterns. (1) Large seasonal variations in the prevalence of patent infections. (2) Evidence from size-prevalence curves that suggests a variable force-of-infection from man to snail, correlated with water temperature. (3) Prevalences of infection that were higher in the vicinity of (+/- 60 m from) major water contact sites. Local prevalences of infection for B. globosus sometimes exceeded 50% and may have approached 100% if pre-patent infections are included. Snail numbers may limit transmission at these locations. Attention is drawn to the need to make field observations at an appropriate spatial scale and also to the implications for the effectiveness of focal snail control as a means of reducing transmission.
146 citations