A circular analysis of chronobiology of Schistosoma japonicum cercarial emergence from hilly areas of Anhui,China

About 46 mammal species have been suspected as reservoir hosts for Schistosoma japonicum and therefore the track of the target parasites, in relation to definitive host species, may be of great importance in terms of theoretical and practical implications. The circadian rhythm of cercariae emergence, a genetically controlled behavior for parasites to adapt to their definitive hosts, may seem to be a perfect biological marker for S. japonicum. In this study, a late (or nocturnal) cercarial emergence pattern was observed on the parasites from one hilly region in Anhui of China, where rodents serve as reservoirs, and on the first generation of the parasites. Moreover, by using the circular statistics, the homogeneity of parasites in such trait was also demonstrated. All these provide evidence for the genetically controlled biological trait, which seems essential in the investigation of macro- or micro-dynamics of parasite transmission of interest. This is particularly true in the case of S. japonicum when multiple parasite isolates or strains are more likely to exist.     

Parasite genetic differentiation by habitat type and host species: molecular epidemiology of Schistosoma japonicum in hilly and marshland areas of Anhui Province, China

Schistosoma japonicum , a parasite of significant public health importance in parts of China and Southeast Asia, is a true generalist pathogen with over 40 species of mammals suspected as definitive host reservoirs. In order to characterize levels of parasite gene flow across host species and identify the most important zoonotic reservoirs, S. japonicum larvae (miracidia) were sampled from a range of definitive host species in two contrasting habitat types within Anhui Province, China: a low-lying marshland region, and a hilly region, where animal reservoir populations may be predicted to differ substantially. Miracidia samples were genotyped using seven multiplexed microsatellite markers. Hierarchical F -statistics and clustering analyses revealed substantial geographical structuring of S. japonicum populations within Anhui, with strong parasite genetic differentiation between habitat types. Within most villages, there was very little or no parasite genetic differentiation among host species, suggesting frequent S. japonicum gene flow, and thus also transmission, across species. Moreover, the data provide novel molecular evidence that rodents and dogs are potentially very important infection reservoirs in hilly regions, in contrast to bovines in the marshland regions. The parasite genetic differentiation between habitat types might therefore be associated with contrasting host reservoirs. The high levels of parasite gene flow observed across host species in sympatric areas have important implications for S. japonicum control, particularly in hilly regions where control of infection among wild rodent populations could be challenging.     

Population Genetics of Schistosoma japonicum within the Philippines Suggest High Levels of Transmission between Humans and Dogs

Background

Schistosoma japonicum, which remains a major public health problem in the Philippines and mainland China, is the only schistosome species for which zoonotic transmission is considered important. While bovines are suspected as the main zoonotic reservoir in parts of China, the relative contributions of various non-human mammals to S. japonicum transmission in the Philippines remain to be determined. We examined the population genetics of S. japonicum in the Philippines in order to elucidate transmission patterns across host species and geographic areas.

Methodology/Principal Findings

S. japonicum miracidia (hatched from eggs within fecal samples) from humans, dogs, pigs and rats, and cercariae shed from snail-intermediate hosts, were collected across two geographic areas of Samar Province. Individual isolates were then genotyped using seven multiplexed microsatellite loci. Wright''s F_ST values and phylogenetic trees calculated for parasite populations suggest a high frequency of parasite gene-flow across definitive host species, particularly between dogs and humans. Parasite genetic differentiation between areas was not evident at the definitive host level, possibly suggesting frequent import and export of infections between villages, although there was some evidence of geographic structuring at the snail–intermediate host level.

Conclusions/Significance

These results suggest very high levels of transmission across host species, and indicate that the role of dogs should be considered when planning control programs. Furthermore, a regional approach to treatment programs is recommended where human migration is extensive.     

Evolution in a multi-host parasite: Chronobiological circadian rhythm and population genetics of Schistosoma japonicum cercariae indicates contrasting definitive host reservoirs by habitat

Schistosomiasis japonica is a disease of profound medical and veterinary importance which has remained endemic in many regions and has re-emerged where previously controlled in China. Although over 40 mammalian species are suspected as reservoirs for Schistosoma japonicum, their relative roles, particularly wildlife, remain to be ascertained. As cercarial emergence is a heritable trait shaped by the definitive hosts’ behaviour, three chronobiological trials of cercarial emergence from field-collected snails from two contrasting ecological regions within China were performed, followed by genetic analyses of the parasites. Two distinct modes were identified, with late afternoon emergence mainly found in the hill region, compatible with a nocturnal rodent reservoir, and early emergence within the marshland consistent with a diurnal cattle reservoir. Furthermore, genetic analyses pointed to a clear separation between cercariae with different biological traits. The phenotypic and genotypic differentiation of the parasites identified here between and within two regions may indicate a strain complex. Such parasite diversity could, in turn, provide an explanation for the different infection scenarios observed between the two regions, and hence have important applied implications in terms of targeted control of key reservoirs.     

Assessing the Effect of an Integrated Control Strategy for Schistosomiasis Japonica Emphasizing Bovines in a Marshland Area of Hubei Province,China: A Cluster Randomized Trial

Introduction

More than 80% of schistosomiasis patients in China live in the lake and marshland regions. The purpose of our study is to assess the effect of a comprehensive strategy to control transmission of Schistosoma japonicum in marshland regions.

Methodology/Principal Findings

In a cluster randomized controlled trial, we implemented an integrated control strategy in twelve villages from 2009 through 2011 in Gong''an County, Hubei Province. The routine interventions included praziquantel chemotherapy and controlling snails, and were implemented in all villages. New interventions, mainly consisting of building fences to limit the grazing area for bovines, building safe pastures for grazing, improving the residents'' health conditions and facilities, were only implemented in six intervention villages. Results showed that the rate of S. japonicum infection in humans, bovines, snails, cow dung and mice in the intervention group decreased from 3.41% in 2008 to 0.81% in 2011, 3.3% to none, 11 of 6,219 to none, 3.9% to none and 31.7% to 1.7%, respectively (P<0.001 for all comparisons). In contrast, there were no statistically significant reductions of S. japonicum infection in humans, bovines and snails from 2008 to 2011 in the control group (P>0.05 for all comparisons). Moreover, a generalized linear model showed that there was a higher infection risk in humans in the control group than in the intervention group (OR = 1.250, P = 0.001) and an overall significant downward trend in infection risk during the study period.

Conclusions/Significance

The integrated control strategy, designed to reduce the role of bovines and humans as sources of S. japonicum infection, was highly effective in controlling the transmission of S. japonicum in marshland regions in China.

Trial Registration

Chinese Clinical Trial Registry ChiCTR-PRC-12002405.     

A Cluster-Randomised Intervention Trial against Schistosoma japonicum in the Peoples' Republic of China: Bovine and Human Transmission

Background

Zoonotic schistosomiasis japonica is a major public health problem in China. Bovines, particularly water buffaloes, are thought to play a major role in the transmission of schistosomiasis to humans in China. Preliminary results (1998–2003) of a praziquantel (PZQ)-based pilot intervention study we undertook provided proof of principle that water buffaloes are major reservoir hosts for S. japonicum in the Poyang Lake region, Jiangxi Province.

Methods and Findings

Here we present the results of a cluster-randomised intervention trial (2004–2007) undertaken in Hunan and Jiangxi Provinces, with increased power and more general applicability to the lake and marshlands regions of southern China. The trial involved four matched pairs of villages with one village within each pair randomly selected as a control (human PZQ treatment only), leaving the other as the intervention (human and bovine PZQ treatment). A sentinel cohort of people to be monitored for new infections for the duration of the study was selected from each village. Results showed that combined human and bovine chemotherapy with PZQ had a greater effect on human incidence than human PZQ treatment alone.

Conclusions

The results from this study, supported by previous experimental evidence, confirms that bovines are the major reservoir host of human schistosomiasis in the lake and marshland regions of southern China, and reinforce the rationale for the development and deployment of a transmission blocking anti-S. japonicum vaccine targeting bovines.

Trial Registration

Australian New Zealand Clinical Trials Registry ACTRN12609000263291     

Body size,trophic level,and the use of fish as transmission routes by parasites

Within food webs, trophically transmitted helminth parasites use predator–prey links for their own transfer from intermediate prey hosts, in which they occur as larval or juvenile stages, to predatory definitive hosts, in which they reach maturity. In large taxa that can be used as intermediate and/or definitive hosts, such as fish, a host species’ position within a trophic network should determine whether its parasite fauna consists mostly of adult or larval helminths, since vulnerability to predation determines an animal’s role in predator–prey links. Using a large database on the helminth parasites of 303 fish species, we tested whether the proportion of parasite species in a host that occur as larval or juvenile stages is best explained by their trophic level or by their body size. Independent of fish phylogeny or habitat, only fish body length emerged as a significant predictor of the proportion of parasites in a host that occur as larval stages from our multivariate analyses. On average, the proportion of larval helminth taxa in fish shorter than 20 cm was twice as high as that for fish over 100 cm in length. This is consistent with the prediction that small fishes, being more vulnerable to predation, make better hosts for larval parasites. However, trophic level and body length are strongly correlated among fish species, and they may have separate though confounded effects on the parasite fauna exploiting a given species. Helminths show varying levels of host specificity toward their intermediate host when the latter is the downstream host involved in trophic transmission toward an upstream definitive host. Given this broad physiological compatibility of many helminths with fish hosts, our results indicate that fish body length, as a proxy for vulnerability to predators, is a better predictor of their use by helminth larvae than their trophic level based on diet content.     

湘江长沙段洲滩钉螺防治后的种群动态

采用以系统抽样结合环境抽查的查螺方法,对湘江长沙段洲滩进行连续6年的螺情调查.2003-2008年跟踪调查了湘江长沙段24个洲滩,其中20个洲滩有钉螺分布,占洲滩总数的83.3%,4个洲滩从未查见钉螺.活螺洲滩数分别占当年调查洲滩的62.50%、66.67%、66.67%、70.83%、33.33%、37.50%;2008年与2003年相比,活螺洲滩数下降了40.00%,有螺框出现率、钉螺平均密度、活螺率分别下降了99.10%、99.74%、51.09%.经统计学处理,各洲滩有螺框出现率(Z=91.56,P<0.01)、活螺率(Z=65.13,P<0.01)不相同,但年度下降趋势明显.在20个有螺洲滩中,有感染性钉螺分布的洲滩5个,占有螺洲滩总数的25.00%;有感染性钉螺分布的洲滩逐年减少,平均密度和感染率逐年降低,2007-2008年所有洲滩均无感染性钉螺分布.湘江长沙段有螺洲滩采取的各种防治措施中,药物与环改灭螺相结合的效果远好于单纯的药物灭螺.各种环改灭螺措施中,又以抬洲降滩、翻耕垦种的灭螺效果更持久,更彻底.2007、2008年有螺洲滩数、钉螺总数急剧减少,有螺框出现率、活螺率大幅度下降还町能与水位和气候有关.湘江长沙段洲滩的螺情得到了较好的控制.     

Microarray Analysis of Gene Expression Profiles of Schistosoma japonicum Derived from Less-Susceptible Host Water Buffalo and Susceptible Host Goat

Background

Water buffalo and goats are natural hosts for S. japonicum in endemic areas of China. The susceptibility of these two hosts to schistosome infection is different, as water buffalo are less conducive to S. japonicum growth and development. To identify genes that may affect schistosome development and survival, we compared gene expression profiles of schistosomes derived from these two natural hosts using high-throughput microarray technology.

Results

The worm recovery rate was lower and the length and width of worms from water buffalo were smaller compared to those from goats following S. japonicum infection for 7 weeks. Besides obvious morphological difference between the schistosomes derived from the two hosts, differences were also observed by scanning and transmission electron microscopy. Microarray analysis showed differentially expressed gene patterns for parasites from the two hosts, which revealed that genes related to lipid and nucleotide metabolism, as well as protein folding, sorting, and degradation were upregulated, while others associated with signal transduction, endocrine function, development, immune function, endocytosis, and amino acid/carbohydrate/glycan metabolism were downregulated in schistosomes from water buffalo. KEGG pathway analysis deduced that the differentially expressed genes mainly involved lipid metabolism, the MAPK and ErbB signaling pathways, progesterone-mediated oocyte maturation, dorso-ventral axis formation, reproduction, and endocytosis, etc.

Conclusion

The microarray gene analysis in schistosomes derived from water buffalo and goats provide a useful platform to disclose differences determining S. japonicum host compatibility to better understand the interplay between natural hosts and parasites, and identify schistosome target genes associated with susceptibility to screen vaccine candidates.     

Genetic diversity of Schistosoma japonicum miracidia from individual rodent hosts

Schistosoma japonicum is an important parasite in terms of clinical, veterinary and socio-economic impacts, and rodents, a long neglected reservoir for the parasite, have recently been found to act as reservoir hosts in some endemic areas of China. Any difference in the host's biological characteristics and/or associated living habitats among rodents may result in different environments for parasites, possibly resulting in a specific population structure of parasites within hosts. Therefore knowledge of the genetic structure of parasites within individual rodents could improve our understanding of transmission dynamics and hence our ability to develop effective control strategies. In this study, we aimed to describe a host-specific structure for S. japonicum and its potential influencing factors. The results showed a significant genetic differentiation among hosts. Two factors, including sampling seasons and the number of miracidia genotyped per host, showed an effect on the genetic diversity of an infrapopulation through a univariable analysis but not a multivariable analysis. A possible scenario of clustered infection foci and the fact of multiple definitive host species, the latter of which is unique to S. japonicum compared with other schistosomes, were proposed to explain the observed results and practical implications for control strategies are recommended.     

Sarcocystis cruzi: comparative studies confirm natural infections of buffaloes

Controversy exists concerning whether cattle and water buffalo sustain infections with cysts of distinct arrays of species in the genus Sarcocystis. In particular, morphologically similar parasites have been alternately ascribed to Sarcocystis cruzi or to Sarcocystis levinei, depending on their occurrence in cattle or water buffalo. We used light and transmission electron microscopy, genetic analysis, and experimental infections of definitive canine hosts to determine whether consistent differences could be identified from parasites derived from several natural infections of each host, examining several tissue types (esophagus, skeletal muscles, and heart). Cysts derived from cattle and water buffalo shared similar structure; variation among 18S rRNA sequences did not segregate consistently according to intermediate host type; parasites derived from cattle and water buffalo induced similar outcomes in the canine definitive host. One cattle specimen harbored unusually large (macroscopic) sarcocysts which nonetheless conformed to previously reported ultrastructural and genetic features of S. cruzi. Finding no consistent basis to differentiate between them, we conclude that the parasites infecting each host and tissue type correspond to S. cruzi. In our sample, no phylogenetically distinct taxon was sampled which might correspond to a distinct taxon previously described as S. levinei. Either that taxon was missed by our sampling effort, or it may represent a junior synonym to S. cruzi, which would then cycle between dogs and a broader range of intermediate bovine hosts than was previously considered.     

Effects of intermediate host genetic background on parasite transmission dynamics: a case study using Schistosoma mansoni

For parasites that require multiple hosts to complete their development, genetic interplay with one host may impact parasite transmission and establishment in subsequent hosts. In this study, we used microsatellite loci to address whether the genetic background of snail intermediate hosts influences life-history traits and transmission patterns of dioecious trematode parasites in their definitive hosts. We performed experimental Schistosoma mansoni infections utilizing two allopatric populations of Biomphalaria glabrata snails and assessed intensities and sex ratios of adult parasites in mouse definitive hosts. Our results suggest that the genetic background of hosts at one point in a parasite’s life cycle can influence the intensities and sex ratios of worms in subsequent hosts.     

Inbreeding within human Schistosoma mansoni: do host-specific factors shape the genetic composition of parasite populations?

The size, structure and distribution of host populations are key determinants of the genetic composition of parasite populations. Despite the evolutionary and epidemiological merits, there has been little consideration of how host heterogeneities affect the evolutionary trajectories of parasite populations. We assessed the genetic composition of natural populations of the parasite Schistosoma mansoni in northern Senegal. A total of 1346 parasites were collected from 14 snail and 57 human hosts within three villages and individually genotyped using nine microsatellite markers. Human host demographic parameters (age, gender and village of residence) and co-infection with Schistosoma haematobium were documented, and S. mansoni infection intensities were quantified. F-statistics and clustering analyses revealed a random distribution (panmixia) of parasite genetic variation among villages and hosts, confirming the concept of human hosts as ‘genetic mixing bowls'' for schistosomes. Host gender and village of residence did not show any association with parasite genetics. Host age, however, was significantly correlated with parasite inbreeding and heterozygosity, with children being more infected by related parasites than adults. The patterns may be explained by (1) genotype-dependent ‘concomitant immunity'' that leads to selective recruitment of genetically unrelated worms with host age, and/or (2) the ‘genetic mixing bowl'' hypothesis, where older hosts have been exposed to a wider variety of parasite strains than children. The present study suggests that host-specific factors may shape the genetic composition of schistosome populations, revealing important insights into host–parasite interactions within a natural system.     

Chance or choice? Understanding parasite selection and infection in multi-host communities

Ongoing debate over the relationship between biodiversity and disease risk underscores the need to develop a more mechanistic understanding of how changes in host community composition influence parasite transmission, particularly in complex communities with multiple hosts. A key challenge involves determining how motile parasites select among potential hosts and the degree to which this process shifts with community composition. Focusing on interactions between larval amphibians and the pathogenic trematode Ribeiroia ondatrae, we designed a novel, large-volume set of choice chambers to assess how the selectivity of free-swimming infectious parasites varied among five host species and in response to changes in assemblage composition (four different permutations). In a second set of trials, cercariae were allowed to contact and infect hosts, allowing comparison of host-parasite encounter rates (parasite choice) with infection outcomes (successful infections). Cercariae exhibited consistent preferences for specific host species that were independent of the community context; large-bodied amphibians, such as larval bullfrogs (Rana catesbeiana), exhibited the highest level of parasite attraction. However, because host attractiveness was decoupled from susceptibility to infection, assemblage composition sharply affected both per-host infection as well as total infection (summed among co-occurring hosts). Species such as the non-native R. catesbeiana functioned as epidemiological ‘sinks’ or dilution hosts, attracting a disproportionate fraction of parasites relative to the number that established successfully, whereas Taricha granulosa and especially Pseudacris regilla supported comparatively more metacercariae relative to cercariae selection. These findings provide a framework for integrating information on parasite preference in combination with more traditional factors such as host competence and density to forecast how changes within complex communities will affect parasite transmission.     

Prevalence and Molecular Phylogenetic Analysis of Severe Fever with Thrombocytopenia Syndrome Virus in Domestic Animals and Rodents in Hubei Province,China

<正>Dear Editor,In 2009, an outbreak of an unknown infectious disease occurred in rural areas of Hubei Province, China, affecting17 persons, five of whom died. It was initially suspected to be human anaplasmosis(Zhang et al. 2008). However, the laboratory evidence was insufficient to verify the diagnosis     

Population Genetics of the Filarial Worm Wuchereria bancrofti in a Post-treatment Region of Papua New Guinea: Insights into Diversity and Life History

Background

Wuchereria bancrofti (Wb) is the primary causative agent of lymphatic filariasis (LF). Our studies of LF in Papua New Guinea (PNG) have shown that it is possible to reduce the prevalence of Wb in humans and mosquitoes through mass drug administration (MDA; diethylcarbamazine with/without ivermectin). While MDAs in the Dreikikir region through 1998 significantly reduced prevalence of Wb infection, parasites continue to be transmitted in the area.

Methods

We sequenced the Wb mitochondrial Cytochrome Oxidase 1 (CO1) gene from 16 people infected with Wb. Patients were selected from 7 villages encompassing both high and moderate annual transmission potentials (ATP). We collected genetic data with the objectives to (i) document contemporary levels of genetic diversity and (ii) distinguish between populations of parasites and hosts across the study area.

Principle Findings

We discovered 109 unique haplotypes currently segregating in the Wb parasite population, with one common haplotype present in 15 out of 16 infections. We found that parasite diversity was similar among people residing within the same village and clustered within transmission zones. For example, in the high transmission area, diversity tended to be more similar between neighboring villages, while in the moderate transmission area, diversity tended to be less similar.

Conclusions

In the Dreikikir region of PNG there are currently high levels of genetic diversity in populations of Wb. High levels of genetic diversity may complicate future MDAs in this region and the presence of dominant haplotypes will require adjustments to current elimination strategies.     

Red List of macrofaunal benthic invertebrates of the Wadden Sea

Parasites were observed in medium- and small-sized fish taken from the discards of a commercial shrimper during seven different cruises in the tidal channels of the North Frisian Wadden Sea (Süderaue, North Sea) from April to September 1991. In total, 442 fish comprising four species (Sprattus sprattus, Hyperoplus lanceolatus, Ammodytes tobianus, Pomatoschistus minutus) were investigated. The parasite fauna consisted of 22 species. The parasite community structure of the 4 hosts was compared. The diet of the hosts seemed to be the main factor determining the structure of the parasite community. Other factors could not be assessed. Eight species of parasites occurred as larval stages. This indicated that fish were intermediate or paratenic hosts in their life cycle. The nematodeHysterothylacium sp. (Anisakidae) and the digeneanCryptocotyle lingua (Heterophyidea) were the dominant parasites, reaching their highest prevalence and density in sprat and sand eel. Sprat and sand eel play a very important role in parasite transmission to predacious fish and seabirds.     

Five-year longitudinal assessment of the downstream impact on schistosomiasis transmission following closure of the Three Gorges Dam

Background

Schistosoma japonicum is a major public health concern in the Peoples'' Republic of China (PRC), with about 800,000 people infected and another 50 million living in areas at risk of infection. Based on ecological, environmental, population genetic and molecular factors, schistosomiasis transmission in PRC can be categorised into four discrete ecosystems or transmission modes. It is predicted that, long-term, the Three Gorges Dam (TGD) will impact upon the transmission of schistosomiasis in the PRC, with varying degree across the four transmission modes.

Methodology/Principal Findings

We undertook longitudinal surveillance from 2002 to 2006 in sentinel villages of the three transmission modes below the TGD across four provinces (Hunan, Jiangxi, Hubei and Anhui) to determine whether there was any immediate impact of the TGD on schistosomiasis transmission. Eight sentinel villages were selected to represent both province and transmission mode. The primary end point measured was human incidence. Here we present the results of this five-year longitudinal cohort study. Results showed that the incidence of human S. japonicum infection declined considerably within individual villages and overall mode over the course of the study. This is also reflected in the yearly odds ratios (adjusted) for infection risk that showed significant (P<0.01) downward trends in all modes over the follow-up period.

Conclusions/Significance

The decrease in human S. japonicum incidence observed across all transmission modes in this study can probably be attributed to the annual human and bovine PZQ chemotherapy. If an increase in schistosome transmission had occurred as a result of the TGD, it would be of negligible size compared to the treatment induced decline seen here. It appears therefore that there has been virtually no immediate impact of the TGD on schistosomiasis transmission downstream of the dam.