Field studies on the transmission of Schistosoma mansoni and on the bionomics of its intermediate host, Biomphalaria glabrata, on St. Lucia, West Indies

Schistosoma mansoni is transmitted by the snail Biomphalaria glabrata on the West Indian island of St. Lucia. A 2$\text{1}\text{2}$-year study of natural snail populations is reported together with simultaneous observations on the transmission of the parasite. Populations in static habitats (pools, marshes and lateral banana drains) were maximal during the rainy part of the year (June–December) but declined during dry spells between January and May. Low infection rates (< 1 %) were observed sporadically in these populations. Higher, more persistent infection rates (5–15%) were obtained in flowing habitat populations (streams and main banana drains) which, however, only became established in periods of low rainfall. The importance of seasonal transmission through flowing habitat colonies was borne out by mouse exposures, supplementary snail studies and human incidence data which between them also gave an insight into the dynamics of transmission. These findings have been used to design a mollusciciding programme as one of several methods of controlling transmission currently being evaluated on St. Lucia.     

Field studies on the bionomics of the free-living stages of St. Lucian Schistosoma mansoni.

Densities of Schistosoma mansoni miracidia and cercariae in natural habitats in three St. Lucian valleys were monitored over a 3-year period by exposure of sentinel snails, Biomphalaria glabrata, and a cercariometric technique, supplemented by sampling of field snails. Separate measures for control of S. mansoni transmission were under evaluation in two of the valleys. Sentinel snails became infected sporadically and their infection rates per valley ranged from 0·12% to 4·99%. S. mansoni miracidial inoculation rates ranged from 1 to over 4 per infected sentinel snail. Combined rainfall of more than 3 in on the day before any day of sentinel snail exposure interfered with miracidium-snail interaction. Densities of S. mansoni cercariae ranged from 0·05 to 21 per litre of water sampled. The number of cercariae detected in a habitat by cercariometry was directly proportional to the number of infected field snails. Sentinel snail infection rates exhibited a downward and an upward trend, respectively, in the controlled and uncontrolled areas, although the changes were not significant statistically.     

Female biased sex-ratio in Schistosoma mansoni after exposure to an allopatric intermediate host strain of Biomphalaria glabrata

For parasites that require multiple hosts to complete their development, the interaction with the intermediate host may have an impact on parasite transmission and development in the definitive host. The human parasite Schistosoma mansoni needs two different hosts to complete its life cycle: the freshwater snail Biomphalaria glabrata (in South America) as intermediate host and a human or rodents as final host. To investigate the influence of the host environment on life history traits in the absence of selection, we performed experimental infections of two B. glabrata strains of different geographic origin with the same clonal population of S. mansoni. One B. glabrata strain is the sympatric host and the other one the allopatric host. We measured prevalence in the snail, the cercarial infectivity, sex-ratio, immunopathology in the final host and microsatellite frequencies of individual larvae in three successive generations.     

Opportunity or catastrophe? effect of sea salt on host-parasite survival and reproduction

Seawater intrusion associated with decreasing groundwater levels and rising seawater levels may affect freshwater species and their parasites. While brackish water certainly impacts freshwater systems globally, its impact on disease transmission is largely unknown. This study examined the effect of artificial seawater on host-parasite interactions using a freshwater snail host, Biomphalaria alexandrina, and the human trematode parasite Schistosoma mansoni. To evaluate the impact of increasing salinity on disease transmission four variables were analyzed: snail survival, snail reproduction, infection prevalence, and the survival of the parasite infective stage (cercariae). We found a decrease in snail survival, snail egg mass production, and snail infection prevalence as salinity increases. However, cercarial survival peaked at an intermediate salinity value. Our results suggest that seawater intrusion into freshwaters has the potential to decrease schistosome transmission to humans.     

Studies on resistance in snails: Interference by nonirradiated echinostome larvae with natural resistance to Schistosoma mansoni in Biomphalaria glabrata

Most of the genetically selected juvenile Biomphalaria glabrata snails, normally strongly resistant to Schistosoma mansoni, lost their juvenile resistance to this parasite when other trematodes were concurrently present in the snail. Three echinostome species all were able to reduce this genetically controlled juvenile resistance: Echinostoma lindoense, E. paraensei, and e. liei. Subsequently, adult resistance to S. mansoni, clearly present in control snails of the same age and strain that were not doubly infected, failed to develop in most of the snails that also harbored echinostomes. Other snails, selected for resistance as adults to S. mansoni, also usually became susceptible to this parasite following infection with E. paraensei. The capacity of E. paraensei to interfere with the snails' resistance to S. mansoni was greater than that of E. lindoense. Destruction by predation of primary sporocysts of S. mansoni by echinostome rediae prevented completion of development of the S. mansoni infections. In a number of snails all primary S. mansoni sporocysts were consumed before secondary sporocysts could be formed. In most experimental snails, however, some of the schistosomes survived, often as a small number of degenerated secondary S. mansoni sporocysts. The capability of flukes to interfere with the natural defense of snails may be an important phenomenon whereby trematode species survive in their snail hosts.     

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.     

Transmission studies of intestinal schistosomiasis in Lake Albert,Uganda and experimental compatibility of local Biomphalaria spp.

Despite ongoing preventive chemotherapy campaigns, intestinal schistosomiasis is hyper-endemic in shoreline communities living along Lake Albert, Uganda. To provide a deeper insight into the local epidemiology of Schistosoma mansoni, a variety of field-based studies were undertaken focusing upon schistosome–snail interactions and confirmation of transmission foci. Cercarial shedding patterns of field-caught Biomphalaria spp., as identified by morphology, were hourly observed over a ten day period and showed that Biomphalaria stanleyi produced significantly more cercariae than Biomphalaria sudanica. Peak production times in both species were between 12.00 and 14.00 h indicating greatest infection risk from lake water exposure is during the early afternoon. Laboratory-bred snails were exposed to locally hatched miracidia and susceptibility of Biomphalaria spp. was confirmed experimentally. Biomphalaria stanleyi was a more permissive host. After ascertaining appropriate conditions for infection of laboratory mice, 28 groups of between 5 and 6 naïve mice were placed in floatation cages at four suspected shoreline transmission sites for a 30 minute period of exposure. Eight weeks later, mice (n = 142) were culled and S. mansoni adult worms were retrieved from 10 animals. Taken as a whole, these observations highlight the local importance of B. stanleyi in transmission of intestinal schistosomiasis and clearly demonstrate the risk of infection on the Lake Albert shoreline. To mitigate this risk local environmental modification(s), i.e. improvement in sanitation and hygiene and control of snail populations, is needed to bolster the impact of chemotherapy-based interventions.     

Host exposure history and priority effects impact the development and reproduction of a dominant parasite

Within a single organism, numerous parasites often compete for space and resources. This competition, together with a parasite’s ability to locate and successfully establish in a host, can contribute to the distribution and prevalence of parasites. Coinfection with trematodes in snail intermediate hosts is rarely observed in nature, partly due to varying competitive abilities among parasite taxa. Using a freshwater snail host (Biomphalaria glabrata), we studied the ability of a competitively dominant trematode, Echinostoma caproni, to establish and reproduce in a host previously infected with a less competitive trematode species, Schistosoma mansoni. Snails were exposed to S. mansoni and co-exposed to E. caproni either simultaneously or 1 week, 4 weeks, or 6 weeks post S. mansoni exposure. Over the course of infection, we monitored the competitive success of the dominant trematode through infection prevalence, parasite development time, and parasite reproductive output. Infection prevalence of E. caproni did not differ among co-exposed groups or between co-exposed and single exposed groups. However, E. caproni infections in co-exposed hosts took longer to reach maturity when the timing between co-exposures increased. All co-exposed groups had higher E. caproni reproductive output than single exposures. We show that although timing of co-exposure affects the development time of parasite transmission stages, it is not important for successful establishment. Additionally, co-exposure, but not priority effects, increases the reproductive output of the dominant parasite.     

Intermediate host specificity in Schistosoma mansoni

Miracidia of Schistosoma mansoni penetrate into many kinds of snails, but development of normal sporocysts takes place only in certain species of Biomphalaria. Different populations of this snail vary greatly in laboratory infection rates with S. mansoni originating from diverse geographic localities. Cross-exposure experiments show that compatibility factors exist in both snails and parasites. Susceptibility of stocks of Biomphalaria to particular strains of S. mansoni is genetically determined and may be modified by selection in the laboratory. In a compatible snail, the sporocyst develops without host tissue reaction; in incompatible snails the early larvae are rapidly surrounded by amebocytes and fibroblasts, and destroyed. This reaction resembles the generalized host cellular response elicited by any foreign body. An individual snail exposed to many miracidia may have both developing and encapsulated sporocysts side by side within its tissues. The weight of current evidence suggests that elicitation or absence of this cellular response resides in the recognition or nonrecognition of the sporocyst as a foreign body. The sporocyst tegument surface, which forms within a few hours after miracidial penetration, may have a molecular conformation identical with that of the snail, or may be able to bind specific host molecules, so that detection and subsequent encapsulation by host cells are averted. Presuming genetic determination of the sporocyst surface structure and of the host cell detection capability, differing infection rates would result from the particular frequencies of relevant genes in the populations concerned.     

Schistosoma mansoni and Biomphalaria glabrata share epitopes: antibodies to sporocysts bind host snail hemocytes

Using an independent protocol, we have confirmed that sporocysts of the human blood fluke, Schistosoma mansoni, synthesize antigens which stimulate rabbit antibody activity to epitopes on infermediate snail host hemocytes. This molecular mimicry may aid S. mansoni to escape the innate immune system of this host, Biomphalaria glabrata.     

Concanavalin A-induced receptor redistribution on Biomphalaria glabrata hemocytes: Characterization of capping and patching responses

Exposure of rounded, glass-adherent hemocytes from a Schistosoma mansoni-susceptible (PR albino) and S. mansoni-refractory (10-R2) stock of snails, Biomphalaria glabrata, to fluoresceinlabeled concanavalin A induces a redistribution of surface membrane Con A receptors. Receptor redistribution (patching and capping) on hemocytes from both snail stocks can be characterized as (1) rapid, with maximum cap formation occurring within 15 min of lectin treatment at 22°C, (2) sodium azide sensitive, but only at relatively high inhibitor concentrations (100–200 mm^?N₃ for capping and 200 mm^?N₃ for patching inhibition), (3) pronase sensitive (partial), but trypsin resistant, and (4) generally unaffected by exposure of snails to S. mansoni miracidia 60 or 180 min prior to extraction of hemolymph (hemocyte) samples for Con A testing. Although differences in the time course of receptor redistribution are exhibited between PR albino and 10-R2 snail hemocytes, the results of experiments involving sodium azide, proteolytic enzymes, and schistosome exposure strongly suggest that Con A-binding determinants and their associated membrane components on rounded hemocytes are very similar in both susceptible and refractory Biomphalaria stocks. It is concluded that if schistosome recognition in refractory 10-R2 snails is mediated through specific hemocyte membrane components, those components associated with Con A reactivity probably are not directly involved in the recognition process.     

The effect of photoperiod inversion upon Schistosoma mansoni cercarial emergence from Biomphalaria glabrata

A delayed pattern of Schistosoma mansoni cercarial emergence from Biomphalaria glabrata is presented, in which cercariae did not emerge from the snail under a diurnal photoperiod until after 12 noon. Even with a reversed (nocturnal) photoperiod, delayed cercarial emergence still persisted.     

Schistosome sporocyst-killing Amoebae isolated from Biomphalaria glabrata.

Explants and swabs from the pericardium and mantle of three strains of Biomphalaria glabrata, two of them resistant to infection with Schistosoma mansoni, have yielded small amoebae, 3–5μm in diameter, in culture. These amoebae have been grown axenically through > 50 passages to date. The amoebae form cysts in dense cultures. When mixed with S. mansoni mother sporocysts in vitro, the amoebae adhere to and kill the trematodes within several hours. For 1–2 days thereafter, the amoebae proliferate rapidly at a generation time of about 5 hr, then return to normal growth. Sonically disrupted sporocysts also induce proliferation. Live sporocysts do not attract the amoebae or emit soluble substances which influence amoebal growth. Amoebae also adhered to and killed S. mansoni daughter sporocysts and cells derived from B. glabrata embryos; however, they did not harm S. mansoni cercariae or rediae of other trematode species. The proportion of mantle explants yielding amoebae was significantly higher (P<0.05) in one of the resistant snail strains than in the susceptible strain; however, whether amoebae contribute to snail resistance is unknown. Exposure of snails to S. mansoni miracidia did not influence the proportion of snails yielding amoebae.     

Control of Schistosoma mansoni transmission: Strategy for using molluscicides on St. Lucia

Control of Schistosoma mansoni transmission: strategy for using molluscicides on St. Lucia. International Journal for Parasitology 3: 795–801. A simplified model, based on previous field studies, is described to summarize the transmission of Schistosoma mansoni on the West Indian Island of St. Lucia by the snail Biomphalaria glabrata. Snail populations in static habitats play little part in transmission but form a reservoir of snails which invade flowing habitats in the dry season. These flowing habitat populations account for most of the transmission: preventing their establishment should greatly reduce transmission. The reasons why a single molluscicide treatment of the static habitat populations is unlikely to achieve this result are discussed and an alternative, practical strategy is suggested. An initial intensive mollusciciding followed by surveillance, coupled with focal mollusciciding of surviving snail colonies, should suppress the static habitat populations sufficiently to prevent the invasion of the flowing habitats. This practical strategy should have a reasonable chance of reducing S. mansoni transmission judging by the results of similar control schemes using molluscicides.     

Schistosoma mansoni: Agglutination of sporocysts,and formation of gels on miracidia transforming in plasma of Biomphalaria glabrata

The resistance or susceptibility of Biomphalaria glabrata strains to strains of Schistosoma mansoni, the human blood fluke, are evidenced by the responses of snail hemocytes to sporocysts of the schistosome, both in vivo and in vitro. It is now reported that living sporocysts of the PR1 strain of S. mansoni agglutinate in the plasma of all tested strains of B. glabrata, in contrast to fixed sporocysts which agglutinate only in plasma from resistant snail strains. The agglutinating activity in resistant plasmas is not divalent cation dependent, and was not inhibited by the 26 carbohydrates and four amino acids tested. In addition, the observation that gelatinous deposits develop on transforming miracidia-sporocysts in B. glabrata plasmas is also reported. Both the agglutination and gel-formation phenomena may facilitate recognition of, and attacks on, sporocysts, thereby contributing to susceptibility and resistance in this host-parasite system.