Snail control strategies for reduction of schistosomiasis transmission

As intermediate hosts, molluscs play a major role in the transmission of schistosomes; they are the sites of an intense multiplication of parasites. Thus, snail control strategies are considered a priority for the reduction of schistosomiasis transmission. Here, Vinca Lardans and Colette Dissous review the efficacy of environmental management and the use of molluscicides and biological agents to control snail populations. They then describe the development of diagnostic tests, based on the detection of parasite antigens or specific parasite DNA sequences in snail tissues, to detect the early infection of snails. Finally, they discuss progress in studying the molecular basis of susceptibility and resistance phenotypes, and the possible application of the genetic manipulation of molluscs.     

Bioenergetic theory predicts infection dynamics of human schistosomes in intermediate host snails across ecological gradients

Epidemiological dynamics depend on the traits of hosts and parasites, but hosts and parasites are heterogeneous entities that exist in dynamic environments. Resource availability is a particularly dynamic and potent environmental driver of within‐host infection dynamics (temporal patterns of growth, reproduction, parasite production and survival). We developed, parameterised and validated a model for resource‐explicit infection dynamics by incorporating a parasitism module into dynamic energy budget theory. The model mechanistically explained the dynamic multivariate responses of the human parasite Schistosoma mansoni and its intermediate host snail to variation in resources and host density. At the population level, feedbacks mediated by resource competition could create a unimodal relationship between snail density and human risk of exposure to schistosomes. Consequently, weak snail control could backfire if reductions in snail density release remaining hosts from resource competition. If resource competition is strong and relevant to schistosome production in nature, it could inform control strategies.     

Biological characteristics and control of intermediate snail host of Schistosoma japonicum

Except for imported cases, we have had no new Schistosoma japonicum infection in Japan since 1977. But there are still two habitats of the intermediate snail host: Oncomelania nosophora in the previous endemic areas of Kofu Basin and Obitsu. O. nosophora from Kofu Basin and Obitsu are susceptible to Chinese and Philippine strains of S. japonicum. The number of immigrants from current endemic areas in China or the Philippines is increasing. In order to prevent re-emerging of S. japonicum infections in Japan, we should continue monitoring on those existing snail hosts and investigate an adequate quarantine system. In Japan, elimination of schistosomiasis has been mainly accomplished by control of the snail host. As measures of snail control, cement-lining of ditches and chemical mollusciciding were most effective in Japan. But the cost of this joint program is too expensive compared with health budget in almost developing countries. In endemic areas of Japan, land reformation from paddy field to fruit farm was also effective. The intermediate snail host in the Philippines, Oncomelania quadrasi is much more aquatic than O. nosophora. For control of O. quadrasi, small drainage of the water and land reclamation from swampy field to rice-field were effective. Based on biological characteristics of Oncomelania spp., we can modify the past successful snail control program in Japan to be adapted ecologically and economically to each endemic area of developing countries.     

Do trematode parasites disrupt defence-cell signalling in their snail hosts?

More than a decade ago, it was postulated that components derived from trematode parasites block receptors on the defence cells of their snail intermediate hosts, thus preventing host-cell activation and parasite elimination. This phenomenon has still not been investigated extensively. However, recent work concerning the molecular regulation of the molluscan defence response provides a new framework for studies that focus on an extension of this original concept - subversion of host cell signalling by trematode parasites. The hypothesis is that, to facilitate survival and replication in their intermediate hosts, trematode parasites down regulate host defence responses by interfering with key signal-transduction pathways in snail defence cells.     

The biological control of snail intermediate hosts of schistosomiasis by fish

Summary The use of molluscivorous fish for biological control of snail intermediate hosts of schistosomiasis is a regularly reappearing theme in the literature on schistosomiasis control. The effectiveness of this control method has not yet been demonstrated, and conclusive field evidence is lacking. In this article the literature on snail control by fish is critically reviewed. Special attention is paid to the cichlid fish Astatoreochromis alluaudi that has been used in well-documented field trials in Kenya and Cameroon. After some small initial success, after a longer period the fish appeared to be ineffective in snail control. Moreover, the fish reproduces at a pace too slow to be of use in large-scale biocontrol trials. Laboratory observations on foraging behaviour and anatomy of the fish give essential cues to explain the failure of the fish in snail control. An observed reduction in the fishes' pharyngeal jaw apparatus, used to crush snails shells, results in a lower profitability of snails. As predicted by a simple foraging model, the prey preference of the fish shifts towards other more profitable prey items, such as benthic and pelagic macrofauna. Although eradication of snails by fish will not be feasible in most cases, the role of natural predators of snails cannot be neglected, and may still be of importance in integrated control efforts.     

Life cycles of the trematode species Azygia hwangtsiytii and A. robusta (Azygiidae) in Primorsky Territory

As a result of experimental and faunistic investigations it is established that the development of the trematode species Azygia hwangtsiytii Tsin, 1933 in Primorsky Territory is realized in the first intermediate host, snail Cipangopaludina ussuriensis, and in second hosts, fishes Perccottus glehni and Channa argus warpachowskii, which can serve as transit, as well as final hosts. For Azygia robusta Odhner, 1911 terms of the development in the first intermediate host, snail Anisus centrifugus are established.     

Spatial covariation between infection levels and intermediate host densities in two trematode species

Both theoretical arguments and empirical evidence suggest that parasite transmission depends on host density. In helminths with complex life cycles, however, it is not clear which host, if any, is the most important. Here, the relationships between the abundance of metacercariae in second intermediate hosts, and the local density of both the first and second intermediate hosts of two trematode species, are investigated. Samples of the snail Potamopyrgus antipodarum, the amphipod Paracalliope fluviatilis and the isopod Austridotea annectens were collected from ten stations in a New Zealand lake. In the trematode Coitocaecum parvum, neither the density of the snail first intermediate host nor that of the amphipod second intermediate host correlated with infection levels in amphipods. In contrast, in the trematode Microphallus, infection levels in isopod second intermediate hosts were positively associated with isopod density and negatively associated with the density of snail first intermediate hosts. These relationships are explained by a negative correlation between snail and isopod densities, mediated in part by their different use of macrophyte beds in the lake. Overall, the results suggest that, at least for Microphallus, local infection levels depend on local intermediate host densities.     

The life cycle and transmission dynamics of the larval stages of Hypoderaeum conoideum

The morphology of the different larval stages and life cycle of Hypoderaeum conoideum (Trematoda: Echinostomatidae) are described. The freshwater snail species Lymnaea peregra (Gastropoda: Lymnaeidae) serves as the natural first intermediate host and this and L. corvus serve as experimental first intermediate hosts. These and other freshwater snails, such as Physella acuta and Gyraulus chinensis, in turn serve as second intermediate hosts. Adult worms were obtained from chicks and ducks, but not from rats, mice and golden hamsters. The morphology of the larval stages is compared with previous work on H. conoideum. Several aspects of the biology of the life history stages are described with emphasis on the transmission dynamics of the free-living stages. Differential suitability of the snail species that may act as first and/or second intermediate hosts is studied and discussed.     

Bird schistosomes: do they die in mammalian skin?

The cercariae of bird schistosomes, released from the intermediate water snail host, actively penetrate the skin of both birds and mammals. Whereas in birds the infection leads to worm maturation and egg production, in the mammalian hosts skin invasion is accompanied by cercarial dermatitis (swimmer's itch, clam-digger's disease) and the fate of the parasites is not clear. Here, we review bird schistosomes as causative agents of cercarial dermatitis, underline adaptations of bird schistosomes to their life in vertebrate hosts, and discuss potential risks caused by the parasites migrating in humans.     

Clonorchiasis: an update

Clonorchis sinensis, the Chinese or oriental liver fluke, is an important human parasite and is widely distributed in southern Korea, China (including Taiwan), Japan, northern Vietnam and the far eastern part of Russia. Clonorchiasis occurs in all parts of the world where there are Asian immigrants from endemic areas. The human and animal reservoir hosts (dogs, pigs, cats and rats) acquire the infection from the ingestion of raw fish containing infectious metacercariae. The first intermediate snail hosts are mainly species of Parafossarulus and Bithynia. Numerous species of freshwater fish serve as the second intermediate hosts of C. sinensis. Extensive studies of clonorchiasis during several decades in Japan, Korea, China and other countries have shown much progress in proving its morphological features including ultrastructure, biology, pathogenesis, epidemiology, clinical manifestations and chemotherapy. The present review deals with mainly current results obtained on the epidemiological, pathological and clinical aspects, as well as control measures in endemic areas. As for the complications of clonorchiasis, formation of calculi in the intrahepatic biliary passages is one of the most characteristic pathological features. It is sometimes accompanied by suppurative cholangitis, cholecystitis, cholangiohepatitis and ultimately can cause cholangiocarcinoma. Experimental results on the relationship to the occurrence of cholangiocarcinoma are presented. Clinical diagnosis by radiological findings including cholangiography, sonography and computerized tomography as well as magnetic resonance imaging for biliary or pancreatic ducts are outlined. Current studies on immunology and molecular biology of C. sinensis were introduced. Praziquantel is the drug of choice for clonorchiasis. The most effective regimen is 25 mg kg(-1) three times daily (total dose, 75 mg kg(-1)) administered orally at 5- to 6-h intervals over a single day. Prevention and control measures are also discussed.     

A schistosomiasis model with an age-structure in human hosts and its application to treatment strategies

We study a system of partial differential equations which models the disease transmission dynamics of schistosomiasis. The model incorporates both the definitive human hosts and the intermediate snail hosts. The human hosts have an age-dependent infection rate and the snail hosts have an infection-age-dependent cercaria releasing rate. The parasite reproduction number R is computed and is shown to determine the disease dynamics. Stability results are obtained via both analytic and numerical studies. Results of the model are used to discuss age-targeted drug treatment strategies for humans. Sensitivity and uncertainty analysis is conducted to determine the role of various parameters on the variation of R. The effects of various drug treatment programs on disease control are compared in terms of both R and the mean parasite load within the human hosts.     

Positive phototropism is accelerated in Biomphalaria glabrata snails by infection with Schistosoma mansoni

Parasite-induced behavioral changes in their hosts favor to complete the lifecycle of parasites. Schistosome infection is also known to cause physiological changes in infected freshwater snail intermediate hosts. Here, we report, a novel phenomenon in which Schistosoma mansoni, a highly debilitating worm affecting millions of people worldwide, alters the phototropic behavior of Biomphalaria glabrata, the vector snail. S. mansoni-infection enhanced positive phototropism of vector snails and infected snails spent significantly more time in light. Possibly, these behavioral changes help the parasite to be released efficiently from the infected intermediate hosts, and to infect mammalian hosts.     

Environmental factors influencing community composition of gastropods and their trematode parasites in southern Ontario

Agricultural activity and landscape features have previously been associated with diversity and prevalence of trematode species in amphibian second intermediate hosts. In this study, the density, diversity, and size of snail first intermediate hosts, and the diversity and prevalence of their trematode species, were assessed in 2 types of ponds, i.e., those adjacent to cornfields and those from the same region in southwestern Ontario that were adjacent to nonagricultural settings. Species of trematodes included, but were not restricted to, those that are known parasites of larval and adult frogs. We also assessed landscape factors likely to influence use by definitive hosts. Presence of the herbicide atrazine in ponds was measured to check that ponds adjacent to agriculture had potential to be affected by agricultural runoff. Both snail size and the proportion of snails releasing cercariae were greater in nonagricultural ponds, contrasting with a previous finding of lower trematode infection in tadpoles from nonagricultural ponds. Percentage of forest cover was associated with prevalence of certain trematode species, but not with estimates of combined prevalence. Absence of relations of trematode prevalence to measures of road density also contrasted with previous studies. We interpret our results in light of how agricultural activity might influence trematode viability, snail growth, and use by wildlife definitive hosts, independently of landscape factors.     

Spatial heterogeneity in recruitment of larval trematodes to snail intermediate hosts

Spatial variation in parasitism is commonly observed in intermediate host populations. However, the factors that determine the causes of this variation remain unclear. Increasing evidence has suggested that spatial heterogeneity in parasitism among intermediate hosts may result from variation in recruitment processes initiated by definitive hosts. I studied the perching and habitat use patterns of wading birds, the definitive hosts in this system, and its consequences for the recruitment of parasites in snail intermediate hosts. Populations of the mangrove snail, Cerithidea scalariformis, collected from mangrove swamps on the east coast of central Florida are parasitized by a diverse community of trematode parasites. These parasites are transmitted from wading birds, which frequently perch on dead mangrove trees. I tested the hypothesis that mangrove perches act as transmission foci for trematode infections of C. scalariformis and that the spatial variation of parasitism frequently observed in this system is likely to emanate from the distribution of wading birds. On this fine spatial scale, definitive host behaviors, responding to a habitat variable, influenced the distribution, abundance and species composition of parasite recruitment to snails. This causal chain of events is supported by regressions between perch density, bird abundance, bird dropping density and ultimately parasite prevalence in snails. Variation between prevalence of parasites in free-ranging snails versus caged snails shows that while avian definitive hosts initiate spatial patterns of parasitism in snails through their perching behaviors, these patterns may be modified by the movement of snail hosts. Snail movement could disperse their associated parasite populations within the marsh, which may potentially homogenize or further increase parasite patchiness initiated by definitive hosts.     

Effects of trematode double infection on the shell size and distribution of snail hosts

Infection with larval trematodes sometimes alters the phenotypes of their snail hosts. While some trematode species have distinct effects on host phenotypes, it is still unclear how snail phenotypes are altered when they are parasitized with multiple trematode species. Here, we report that double infection with trematode species averages the effects of parasitic alteration on host phenotype. We found that snail hosts Batillaria attramentaria (Batillariidae) infected with Cercaria batillariae (Heterophyidae) have abnormally large shells and distribute in lower areas of the intertidal zone. Snails with another dominant trematode species, the renicolid cercaria I (Renicolidae), have slightly larger shells and distribute in upper areas of the intertidal zone. A number of double infections with both trematodes was observed in this study. Snails infected with both trematode species exhibited an intermediate size and inhabited a depth between those of snails solely infected with either trematode species, suggesting that the two trematodes simultaneously affected the snail phenotypes. Because altered host phenotypes are frequently beneficial to parasites, two trematode species may compete for successful transmission through alteration of host phenotypes.     

Trichobilharzia ocellata: physiological characterization of giant growth, glycogen depletion, and absence of reproductive activity in the intermediate snail host, Lymnaea stagnalis

Giant growth, depletion of energy stores, and inhibition of reproductive activity are striking effects of many trematode parasites on their intermediate snail hosts. Two hypotheses have been put forward to explain these phenomena: (1) host and parasite compete for energy rich and other essential nutrients, with the parasite as the winner, and (2) the parasite intervenes in the endocrine control of reproduction of the snail. These hypotheses were tested in the present study with the Trichobilharzia ocellata/Lymnaea stagnalis association. The snails were infected at a juvenile stage, and release of cercariae started on Day 55 after exposure. It was shown that enhanced growth of infected snails is not paralleled by a greater increase in dry weight, but hemolymph volume does increase, being 35% greater than in the noninfected controls. Control snails, on the other hand, showed an increase in the percentage body dry weight during sexual maturation. The conclusion is that infected snails retain an essentially juvenile body structure. In control snails, glycogen was depleted from the mantle store at the start of egg laying but the onset of cercariae production marked a severe glycogen depletion from the headfoot and the mantle in infected snails, being nearly complete on Day 68 after exposure. The hemolymph glucose concentration was only slightly lower in infected than in control snails and it did not change (in both groups) during glycogen mobilization. This suggests that glycogen mobilization does not result from the snail and the parasite competing directly for metabolites within the hemolymph. Infection inhibited the maturation of the accessory sex organs: there was no increase in the relative wet weights nor in the amounts of DNA and secretion products in the albumin and prostate glands. Infected snails did not lay eggs. It is presumed that the parasite produces one or more agents which intervene in the action of the gonadotrophic hormones. The release of these agents commences at an early stage of infection.     

Of mice and worms: are co-infections with unrelated parasite strains more damaging to definitive hosts?

Intraspecific competition between co-infecting parasites can influence the amount of virulence, or damage, they do to their host. Kin selection theory dictates that infections with related parasite individuals should have lower virulence than infections with unrelated individuals, because they benefit from inclusive fitness and increased host longevity. These predictions have been tested in a variety of microparasite systems, and in larval stage macroparasites within intermediate hosts, but the influence of adult macroparasite relatedness on virulence has not been investigated in definitive hosts. This study used the human parasite Schistosoma mansoni to determine whether definitive hosts infected with related parasites experience lower virulence than hosts infected with unrelated parasites, and to compare the results from intermediate host studies in this system. The presence of unrelated parasites in an infection decreased parasite infectivity, the ability of a parasite to infect a definitive host, and total worm establishment in hosts, impacting the less virulent parasite strain more severely. Unrelated parasite co-infections had similar virulence to the more virulent of the two parasite strains. We combine these findings with complementary studies of the intermediate snail host and describe trade-offs in virulence and selection within the life cycle. Damage to the host by the dominant strain was muted by the presence of a competitor in the intermediate host, but was largely unaffected in the definitive host. Our results in this host–parasite system suggest that unrelated infections may select for higher virulence in definitive hosts while selecting for lower virulence in intermediate hosts.     

Schistosomiasis research in the dongting lake region and its impact on local and national treatment and control in China

Schistosomiasis is a chronic and debilitating parasitic disease that has often been neglected because it is a disease of poverty, affecting poor rural communities in the developing world. This is not the case in the People's Republic of China (PRC), where the disease, caused by Schistosoma japonicum, has long captured the attention of the Chinese authorities who have, over the past 50-60 years, undertaken remarkably successful control programs that have substantially reduced the schistosomiasis disease burden. The Dongting Lake region in Hunan province is one of the major schistosome-endemic areas in the PRC due to its vast marshland habitats for the Oncomelania snail intermediate hosts of S. japonicum. Along with social, demographic, and other environmental factors, the recent completion and closure of the Three Gorges dam will most likely increase the range of these snail habitats, with the potential for re-emergence of schistosomiasis and increased transmission in Hunan and other schistosome-endemic provinces being a particular concern. In this paper, we review the history and the current status of schistosomiasis control in the Dongting Lake region. We explore the epidemiological factors contributing to S. japonicum transmission there, and summarise some of the key research findings from studies undertaken on schistosomiasis in Hunan province over the past 10 years. The impact of this research on current and future approaches for sustainable integrated control of schistosomiasis in this and other endemic areas in the PRC is emphasised.     

Development of Trichobilharzia australis Blair & Islam, 1983 in the snail, Lymnaea lessoni Deshayes and in an experimental definitive host, the Muscovy duck

The development of Trichobilharzia australis Blair & Islam, 1983 in the intermediate host, Lymnaea lessoni Deshayes and in experimental definitive hosts, Muscovy ducks is described. 24 hours after entry into the snail, miracidia had lost their cilia, epidermal plates and lateral processes and became young mother sporocysts. They were located in the tissues of the head-foot organ of the snail and were oval in cross section but still retained the shape of a miracidium, and measured 0.058-0.066 X 0.041-0.049 mm. From the seventh day onward young mother sporocysts were tubular, thin-walled, irregular in shape and were in the tissues of the lung and kidney of the snail. On the 24th day mature mother sporocysts and young daughter sporocysts were found in the digestive gland. Between the 24th and 29th day mature daughter sporocysts with fully developed cercariae ready to emerge, or already emerged, could be seen in the digestive gland of the snail. Cercariae emerged from the snail from the 29th to 46th day after exposure at 25 degrees +/- 1 degree C. The prepatent period of T. australis in the Muscovy ducks was 22 to 42 days after the beginning of exposure to cercariae.     

Effects of ultraviolet radiation on the transmission process of an intertidal trematode parasite

The transmission of parasites takes place under exposure to a range of fluctuating environmental factors, one being the changing levels of solar ultraviolet radiation (UVR). Here, we investigated the effects of ecologically relevant levels of UVR on the transmission of the intertidal trematode Maritrema novaezealandensis from its first intermediate snail host (Zeacumantus subcarinatus) to its second intermediate amphipod host (Paracalliope novizealandiae). We assessed the output of parasite transmission stages (cercariae) from infected snail hosts, the survival and infectivity of cercariae, the susceptibility of amphipod hosts to infection (laboratory experiments) and the survival of infected and uninfected amphipod hosts (outdoor experiment) when exposed to photo-synthetically active radiation only (PAR, 400-700 nm; no UV), PAR+UVA (320-700 nm) or PAR+UVA+UVB (280-700 nm). Survival of cercariae and susceptibility of amphipods to infection were the only two steps significantly affected by UVR. Survival of cercariae decreased strongly in a dose-dependent manner, while susceptibility of amphipods increased after exposure to UVR for a prolonged period. Exposure to UVR thus negatively affects both the parasite and its amphipod host, and should therefore be considered an influential component in parasite transmission and host-parasite interactions in intertidal ecosystems.