Impact of Schistosoma sp., infection on biological, behavioral, physiological, histological, and genotoxicological aspects of Biomphalaria alexandrina and Bulinus truncatus snails

doi:10.21203/rs.3.rs-3110632/v1

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Impact of Schistosoma sp., infection on biological, behavioral, physiological, histological, and genotoxicological aspects of Biomphalaria alexandrina and Bulinus truncatus snails

https://doi.org/10.21203/rs.3.rs-3110632/v1

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published 01 Feb, 2024

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Trematodes infection of genus Schistosoma can lead to physiological and behavioral changes in intermediate snail hosts. This is because the parasite consumes essential resources required for the host's survival, but the hosts can adaptively modify their behavior to ensure some level of fitness before parasite-induced mortality. The present study examined the reproductive and biochemical parameters of Biomphalaria alexandrina and Bulinus truncatus during the shedding stage of infection with Schistosoma mansoni and haematobium, respectively. The study found that the infection rate with S. mansoni was 34.7% and 30.4% with S. haematobium. In B.alexandrina infected with S. mansoni, a survival rate of 65.2% was recorded, along with a mean duration of shedding of 32.8 ± 5.5 days, a mean prepatent period of 37.5 ± 1.15 days, and a mean life span of 57.0 ± 1.21 days. Meanwhile, in B. truncatus infected with S. haematobium, a survival rate of 56.4% was recorded, with a mean duration of shedding of 42.6 ± 2.6 days, a mean prepatent period of 46.7 ± 2.3 days, and a mean life span of 65.9 ± 1.6 days.

The feeding behavior was increased in the two infected species snail, while the net reproductive rate (R_o) of the infected species snails was reduced. Total antioxidant (TAO) and lipid peroxidation activity were increased in the two infected snails during shedding, while Glutathione-S-transferase was reduced. Lipid peroxidase (LPO) activity and nitrogen oxide (NO) levels decreased significantly in infected B. alexandrina and increased in infected Bulinus. Steroid hormone measurements were increased in the infected Biomphalaria, while they were reduced in infected Bulinus. Comet assay parameters were increased in the two infected genera after infection than control snails, and histopathological damage occurred. These observations demonstrated that infection initiates diverse biochemical, hormonal, genotoxic, and histopathological change to the tissues responsible for fecundity and reproduction in B. alexandrina and B. truncatus.

Biomphalaria alexandrina

Bulinus truncatus

genotoxic effect

food behavior

Schistosoma haematobium

Schistosoma mansoni

Schistosomiasis is a chronic parasitic disease caused by trematodes of the genus Schistosoma, and it is considered the second most devastating disease in terms of morbidity and mortality worldwide (Ibrahim et al., 2023b; WHO 2023). This disease is prevalent in tropical and subtropical areas, affecting approximately 240 million people worldwide, with about 700 million people at risk, especially in poor communities with inadequate sanitation facilities (WHO 2022; Ibrahim et al. 2023a) (WHO 2001, 2011, 2013, and 2012–2020) and (Obare et al., 2016). Schistosoma mansoni and S. haematobium are the two parasites that cause the most widespread forms of intestinal and urogenital schistosomiasis (Mansour and Ibrahim 2023). In our laboratory, we use the infection of B. alexandrina with S. mansoni and B. truncatus with S. haematobium to study the impact of host-parasite infection on physiological and behavioral changes, including reduced fecundity and increased feeding behavior in the two intermediate host species. When B. alexandrina becomes infected with S. mansoni and B. truncatus becomes infected with S. haematobium, the development of the hermaphroditic reproductive system of the two snail species is severely retarded (Joosse and Van 1986, McClelland and Bourns 1969, and Sluiters et al. 1980), resulting in the production of almost no eggs. Numerous studies have reported behavioral alterations in hosts, such as changes in feeding and crawling behavior, caused by parasitic infection, and have interpreted these changes as induced adaptations by parasites to facilitate transfer to the next-stage hosts (Swennen 1969, Curtis 1990, 1993, Levri and Lively 1996). Increased feeding with infection has been interpreted as compensating for nutrient deprivation caused by parasites or as a modification of the host's growth rate (gigantism) (Minchella 1985, Hurd 1990). The comet assay has several advantages over other DNA damage methods, such as sister chromatid exchange, alkali elution, and micronucleus assay, due to its high sensitivity and the fact that DNA strand breaks can be determined in individual cells (Pavlica et al. 2001) (Ibrahim et al. 2018; Morad et al. 2022). Gastropod snails have been reported to be vectors of certain larval digeneans (Choubisa and Sharma 1986; Abdel-Tawab et al. 2022). These snails harbor various developmental stages, such as sporocysts, rediae, and cercariae of adult trematodes. During their multiplication and growth, they obtain nutrients from infected tissues, such as the digestive gland and gonads, leading not only to diverse histopathological changes in the snails but also to physiological disturbances (Huffman and Fried 1985; Soomro et al. 2005; Huffman et al. 2009; Abdel-Tawab et al. 2022; Morad et al. 2022). The aim of this study was to extend and update existing information on the behavioral alterations of hosts (feeding and fecundity) caused by parasitic species, using the B. alexandrina-S. mansoni and B. truncatus-S. haematobium models. Biochemical, histopathological, and genotoxic parameters were measured in homogenate tissue of both infected snails and compared to uninfected snails.

2.2. Species snails with infections:

Juvenile specimens of both B. alexandrina (shell diameter 3-5mm) and B. truncatus (shell diameter 3-5mm) were obtained from the stock reared in the Medical Malacology Department at Theodor Bilharz Research Institute (TBRI), Imbaba, Giza, Egypt. The snails were originally collected from field populations in Giza Governorate and were used for all experiments. The snail species were bred under standard conditions according to Van der et al. (1969). To obtain infections, triplicate groups of 10 B. alexandrina snails were individually exposed to 5–8 freshly hatched S. mansoni miracidia, and triplicate groups of 10 B. truncatus snails were individually exposed to 8–15 freshly hatched S. haematobium miracidia for 3 hours at 25°C in 2 ml vials containing dechlorinated tap water, according to the protocol described by Sluiters et al. (1980) Miracidia of S. mansoni and S. haematobium were obtained from the Schistosome Biological Supply Center (SBSC) at Theodor Bilharz Research Institute in Egypt. Triplicate groups of 10 control snails were individually placed in 2 ml vials without exposure to miracidia. Groups of infected and control snails were kept in plastic aquaria (10 snails per container, with a size of 16 x 23 x 9 cm) containing dechlorinated water. The infected snails were allowed to develop for four weeks after infection with B. alexandrina and eight weeks after infection with B. truncatus. The infection rate was calculated in B. alexandrina four weeks after infection and in B. truncatus eight weeks after infection, following the method by Coles (1973): Infection rate = (number of infected snails/total number of snails examined) x 100. The survival rate at shedding was also calculated for both snail species according to Frank (1963) by the following equation: survival rate = \(\frac{\text{N}\text{u}\text{m}\text{b}\text{e}\text{r} \text{o}\text{f} \text{s}\text{u}\text{r}\text{v}\text{i}\text{v}\text{e}\text{d} \text{s}\text{p}\text{e}\text{c}\text{i}\text{e}\text{s} \text{s}\text{n}\text{a}\text{i}\text{l}\text{s}}{total number of exposed miracidia species snails} x100\) Furthermore, the mean total number of cercariae, means duration of shedding, mean prepatent period, and mean lifespan were calculated for each species of positive infection, using the approach by Moukrim et al., (1995).

2.3. Feeding behavior:

About 10 snails of the same size (8-9mm) from each species infected and control groups were housed in a plastic container (16 × 23 × 9 cm) and provided with 50 circle of washed clean fresh lettuce leaves measuring 4 mm². The snails' were starved before the experiment for one day and then the food was given (Valarmathi 2017). The consumption of the lettuce circles were counted and recorded each day and the number of survived in both snails species was counted (Colpaert et al., 2021). Trireplicate of each species group were done and assessed side by side with the control ones.

2.4. Biological parameters:

To examine the fecundity of the two snail species, pieces of Styrofoam sheets (5 × 5 cm with 0.5 cm thickness) were used as substrates for oviposition, floating on the water surface of a plastic container. Egg masses were collected weekly for four to eight successive weeks. The survivorship of the snails (Lx) and the total number of eggs laid per snail (Mx) were recorded weekly for each aquarium. The reproductive rate (Ro) was calculated at the end of the experiment, according to the method described by Costa et al. (2004).

3. Species snail tissue homogenates and biochemical estimations:

To examine changes in biochemical parameters TAO, LPO, SOD, NO, and GST in two snail species, 500 juvenile snails with an average shell diameter of 7 to 11 mm at the shedding stage were carefully crushed between two glass slides, and their shells were removed. 0.1 g of tissue from each species was weighed and homogenized in 1 ml of phosphate buffer (pH 7.1), then centrifuged at 4000 rpm for 15 minutes, and the supernatant was collected in Eppendorf tubes and stored at -20°C. The supernatants were used for different biochemical analyses. Biodiagnostic kits (Biodiagnostic Dokki, Giza, Egypt) were used to determine SOD (Damerval et al., 1986) and GST (Beutler 1963) levels. Tissue malondialdehyde (lipid peroxide) was assessed according to Ohkawa et al. (1979). Nitric oxide (NO) concentration was determined using a colorimetric NO kit (Biodiagnostic Company, Dokki, Giza, Egypt; Cat. No. GR 2511) based on the method described by Montgomery and Dymock (1962), and total antioxidant capacity was estimated using a kit (Cat. No. TA 2513) according to Koracevic et al. (2001).

3.1. Steroid sex hormones (testosterone and 17β-estradiol)

The levels of steroid hormones, specifically testosterone and 17β-estradiol, were examined in the tissues of two species of snails: one infected and another uninfected (control group). Hormone levels were assayed for all groups of species tested using the T EIA kit from Enzo Life Science (Michigan, USA, ADI-900-065) and the E EIA kit from Cayman Chemical Company (Michigan, USA, item no. 582251) following the manufacturer's instructions (Ibrahim et al., 2023).

3.2. Genotoxicity by Comet assay:

Species snail (7–9 mm) that positive infection with species of trematode at shedding stage as well as control species group were determined to compare DNA damage by single cell gel assay according to Singh et al.. (1988) and Grazeffe et al., (2008).

3.3. Histopathological alterations:

Simultaneous positive infection of B. alexandrina with S. mansoni and B. truncatus with S. haematobium and their respective control groups were carried out. Three replicates of 10 snails/L were used for both the control species and the positive infected species. The snails' digestive and hermaphrodite glands were dissected from their shells, fixed using Bouin's fixative, and embedded in wax blocks. The sections (5–8µm) were then stained with haematoxylin and eosin, following the protocol by Mohamed and Saad (1990). Similarly, sections of the control snails' digestive and hermaphrodite glands were also prepared.

3.4. Statistical analysis:

The values of biological and biochemical parameters were expressed as mean ± SD. The student's "t" test was used to determine significant changes between the means of control and infected groups, following the method by Sakal and Rohlf (1995). The limit for statistical significance was set at p < 0.05, corresponding to a confidence level of 95%.

4.1. Snail’s infection rate:

Infection rate in B. alexandrina with S. mansoni was recorded 34.7% (Fig. 1-A) while recorded 30.4% in B.truncatus with S. haematobium.

4.2. Snail’s duration of shedding and prepatent period:

Duration of shedding varied from 21 to 37 days (Mean: 23.8 ± 5.5) in B. alexandrina and from 18 to 40 days (Mean: 24.6 ± 2.6) for B. truncatus. Prepatent period was 32 days post-infection for B. alexandrina and 46 days post-infection for B. truncatus (see Fig. 1-B).

4.3. Mean total number of cercariae per snails:

The mean number of crecariae per snail Fig. (1-C) in B. alexandrina was 2297.4 ± 272.5 (p < 0.01) and recorded 1637.3 ± 307.5) (p < 0.01) in positive B. truncatus .

4.4. Snail’s mean life span:

It is worth mentioning that the mean lifespan was recorded as 57.0 ± 1.21 days in B. alexandrina (see Fig. 1-D) and 65.9 ± 1.6 days in B. truncates.

4.5. Snail’s survival rate at first shedding:

The survival rate of B. alexandrina exposed to Schistosoma mansoni at first cercarial shedding was 65.2%, while the survival rate of B. truncatus exposed to S. haematobium was 56.4%, as compared to the survival rate in the respective control groups (refer to Fig. 2-A).

4.6. Impact of Schistosoma mansoni with Biomphlaria alexandrina and S haematobium with Bulinus truncatus on feeding behaviour, fecundity and reproductive rate.

During the prepatent period, the number of feeding B. alexandrina snails for green circles of fresh lettuce leaves exceeded that of their uninfected counterparts, indicating that the infected snails were more voracious feeders (see Fig. 2-B). The same pattern was observed in B. truncatus infected with S. haematobium (Fig. 2-C). Additionally, the fecundity of B. alexandrina showed a pattern of ceasing egg-laying for 4 weeks during the prepatent period (see Fig. 2-D), which was also observed in B. truncatus after being exposed to miracidia for 7 weeks(see Fig. 2-E). The net reproductive rate (Ro) in infected B. alexandrina and B. truncatus was significantly reduced to 47.7% and 84.6% of its value in the respective control groups (refer to Fig. 2-F).

5. Impact of infection with Schistosoma mansoni in Biomphlaria alexandrina and infection with S haematobium in Bulinus truncatus on oxidative stress paremeters at 1st shedding stage.

Schistosomiasis mansoni and S. haematobium infection impacted the levels of TAO, LPO, NO, SOD, and GST in the homogenized tissue of infected B. alexandrina and B. truncatus at the shedding stage. TAO activity showed a significantly higher value (p < 0.05) post 32 days of infection in the homogenized tissue of B. alexandrina as compared to the uninfected group, and the same result was recorded post 46 days of infection in infected B. truncatus snails (refer to Fig. 3-A). This suggests that the infections were stressful for the snails. Lipid peroxidation (LPO) activity showed a significant reduction in infected B. alexandrina snails relative to the value in uninfected snails, while in B. truncatus snails, LPO activity increased significantly compared to the control group (refer to Fig. 3-B). Meanwhile, a significant elevation in the levels of NO was observed in tissue homogenate of B. truncatus snails post 46 days of infection, while the level of NO in infected B. alexandrina snails recorded a significant reduction post 32 days of infection as compared to the uninfected group of snails (refer to Fig. 3C). Superoxide dismutase (SOD) levels in infected B. alexandrina and B. truncatus snails were higher than those in uninfected snails in both species (refer to Fig. 3-D). The highest Glutathione-s-transferase (GST) value was measured in infected B. truncatus snails post 46 days of infection, while B. alexandrina snails post 32 days of infection revealed a reduction compared to uninfected B. alexandrina snails (refer to Fig. 3-E). This could be due to the differences in the antioxidant system response in laboratory-infected snail species or the longer prepatent period in B. truncatus (46 days) as compared to B. alexandrina (32 days), regardless of the parasite species.

5.1. Impact of S. mansoni with B. alexandrina and S. haematobium with B. truncatus on 17β-esteradiol and testosterone hormones in tissues at 1st shedding stage.

In infected B. alexandrina snails, the production of cercariae resulted in significant increases in the concentration of 17β-estradiol and testosterone in homogenized tissues at 32 days post-infection (refer to Fig. 4-A), while in infected B. truncatus snails, there was a significant reduction in the concentration of 17β-estradiol and testosterone hormones post 46 days post-infection compared to their concentration in non-infected control snails (p < 0.05) (refer to Fig. 4-B).

6. Impact of S. mansoni with B. alexandrina and S. haematobium with B. truncatus on comet assay at 1st shedding stage.

The comet assay was used to monitor DNA damage in B. alexandrina and B. truncatus snails infected with Schistosoma mansoni and S. haematobium, respectively. Tailed % and tailed length, which indicate cell malformation, showed significant increases in infected B. alexandrina snails as compared to uninfected groups (refer to Fig. 5 & plate 1). Meanwhile, the normal % DNA in the tail that migrated from the head increased in infected B. alexandrina snails. The tail moment, which is a parameter resulting from the tail length and its containing % DNA migrated from the head, may indicate negative impact on the resistance system cell genotoxicity (refer to Fig. 5& plate 1). Olive tail moment, which indicates DNA fragmentation, was significantly increased in infected B. alexandrina snails as compared to the control group (p < 0.05). The same negative impact on comet assay parameters was observed in infected B. truncatus snails with S. haematobium at the shedding stage (refer to Fig. 5 & plate 1).

7. Impact of S. mansoni with B. alexandrina and S. haematobium with B. truncatus on the snails’ digestive and hermaphrodite glands histology at shedding stage.

Infection of B. alexandrina and B. truncatus snails with S. mansoni and S. haematobium, respectively, can have destructive effects on the snail tissues. Histological studies were conducted on sections from the digestive and hermaphrodite glands of both infected and uninfected snails. The normal histological structure of the digestive gland in both species includes two main types of cells: the digestive cells, which are columnar with rounded apices, and the secretory cells, which are pyramidal in shape (refer to Plate 2, A & C). Histological examination of the sections from the digestive gland of infected snails at the shedding stage showed deleterious effects, such as swelling and deformation of the secretory cells, rupturing and disintegration of the digestive cells, and spore capsule of cercariae species (refer to Plate 2, B & D). In the hermaphrodite gland, which produces both male and female reproductive gametes, mature ova are located at the periphery of the acinus, and bundles of male sperms are arranged in the center. Various stages of sperm and ova development are evident simultaneously (refer to Plate 2, A & C). Histological sections of this gland from infected snails revealed varying degrees of degeneration in ova and sperms, depending on the spore capsule of cercariae species during the experimental period of shedding in both species (refer to Plate 2, B & D).

8.1.Snail’s infection rate:

Lab observations of B. alexandrina with S. mansoni and B. truncatus with S. haematobium agreed with Makanga's (1981) finding of 30% IR in young B. pfeifferi with S. mansoni, but differed from Southgate et al., (2000) and Ibikounlé et al., (2012) who reported higher IR in B. pfeifferi with S. mansoni. B. truncatus showed a 50.5% IR for one to seven-day-old snails and 19.9% for snails aged one and a half to five weeks in lab conditions (Moore et al., 1953).

8.2. Snail’s duration of shedding and prepatent period:

The mean prepatent period for B. alexandrina and B. truncatus corresponded to Kechemir and Combes' 1982 findings of 41–56 days and; Pflüger et al., 1984.

8.3. Mean total number of cercariae per snails:

The total number of cercariae/snail counted in this study was different than that reported by Kechemir and Combes (1982) and Kechemir (1985) in B. glabrata. It also concords with those reported in Bulinus truncatus infected by miracidia (from 29 to 65 days at 24–26°C: Lo 1972; Kechemir and Combes 1982; Pflüger et al., 1984). Cercarial emission peaks are adapted to the definitive host's behavior to increase their chance of infection and allow the continuation of the parasite cycle (Kengne-Fokam et al., 2018).

8.4. Snail’s mean life span:

The life-span of cercaria-positive snails was 45–81 days (mean: 57.0 ± 1.2) for B. alexandrina and 55–91 days (mean: 65.9 ± 1.6) for B. truncatus. Archibald (1933) reported a cercaria-positive B. truncatus surviving for four and a half months. Once a digenetic trematode miracidium successfully colonizes a compatible snail host, it initiates a complex proliferative development program that can last for weeks and produce cercariae that persist for the remainder of the infected snail's life span (Hanington et al., 2010).

Currently, no hypothesis can account for the discordance in the prepatent, shedding, and life span period due to differing experimental conditions (molluscan age, size, mode of infection) in other studies. Snails actively shedding Echinostoma spp. cercariae were not different in size from non-shedding, egg-laying snails but had a higher mortality rate (Marchand et al., 2020).

8.5. Snail’s survival rate at 1st shedding stage:

This study reported a reduction in the survival rate of two snail species upon shedding cercariae, which agrees with Mangal et al., (2010) who observed lower survival rates in snails exposed to S. mansoni miracidia compared to unexposed snails. Previous laboratory studies estimating the increase in mortality rates of schistosoma-infected snails compared to uninfected snails is highly variable but can be up to 0.100 (Anderson et al., 1982). Woolhouse (1989) found that patent infections of S. species increased per capita mortality rates of Bulinus globosus and B. pfeifferia, including mortalities during the prepatent period in two infected species. Reduction in this biological parameter may due to potential competition between the parasites and host for essential haemolymph-born nutrients (Becker, 1980) and, may be attributed to histopathogenic effects on the snail host and depletion of nutrient by the parasite especially near the time of the maturation of infection and shedding of cercariae (El-Sayed et al., 1999).

8.6. Impact of Schistosoma infection on feeding behaviour, fecundity and reproductive rate:

Infected B. alexandrina and B. truncatus tended to feed more frequently than uninfected snails. This agrees with Shinagawa et al., (2001) who found that freshwater snails infected with larval trematodes tended to feed more frequently during the light period under laboratory conditions. Parasite infection often results in changes to host behavior, which can represent adaptive manipulation of the host behavior by the parasite to maximize its transmission success (Moore, 2002; Poulin, 2010; Thomas, Adamo, & Moore, 2005). Increased feeding with infection has been interpreted as compensating for the nutrient deprivation caused by parasites or as a modification of the host's growth rate, such as gigantism (Minchella 1985, Hurd 1990). Other researchers have referred to the loose fecundity in infected snails as castration, suggesting that the trematode parasite removes the energetic demands of reproduction, allowing the host to invest this energy towards other life history traits, such as growth and survival (Poulin, 2006; Lafferty and Kuris, 2009). Another possible reason for increased feeding may be starvation autolysis due to squeezing of digestive tubules at different loci, which prevents food from passing into the tubules. This may lead to intracellular digestion, and atrophy of digestive tubules can occur in heavy infection (Mohandas, 1974; Choubisa, 1988). Infection with S. mansoni or S. haematobium miracidia caused B. alexandrina and B. truncatus snails to cease egg-laying post-exposure, resulting in a reduction in reproduction (Joosse and Van 1986, McClelland et al. 1996, Sluiters et al. 1980). The development of the hermaphrodite reproductive system of L. stagnalis infected with T. ocellata was severely retarded, resulting in almost no eggs being produced (Joosse and Van 1986, McClelland et al., 1996, Sluiters et al. 1980, Thornhill et al. 1986). Reductions in fecundity were also observed in three Bulinus species infected with S. haematobium (Fryer et al. 1990). Nutrient deprivation caused by the parasite or the double burden of producing eggs and parasites not borne by the snail may be responsible for reductions in egg-laying (Neuhaus 1949, McClelland and Bourns 1969, Meier and Meier-Brook 1981, Alberto-silva et al. 2015). In our present study, infected snails ceased egg-laying during the early weeks of infection, resulting in a significant reduction in the mean number of eggs per snail in two species. This agrees with Meier and Meier-Brook (1981), who related the suppression in egg-laying to the indirect effect of trematode larvae on oogenesis, possibly due to nutrient withdrawal by the parasite or the double burden of producing eggs and parasites (Neuhaus 1949, McClelland and Bourns 1969). Nutrient deprivation may be responsible for the reduction in egg-laying, which coincides with the development of sporocysts in the digestive gland (Looker and Etges 1979). The presence of a small number of mother sporocysts in the stage of infection may be sufficient to disturb reproductive processes in the two species.

8.7. Impact of Schistosoma infection on oxidative stress paremeters at 1st shedding stage.

Increasing the level of TAO in infected B. alexandrina and B. truncatus snails may explain the increase in the number of haemocytes and generation of large volumes of ROS for defensive purposes to damage or kill the parasite's larvae (Bikowska 2006, Saboor-yaraghi et al., 2011, Hadas´ and Stankiewicz 1996, Mone et al. 2011). Gornowicz et al. (2013) found significant differences in TAS between control and P. elegans-infected Lymnaea stagnalis during the initial period of the experiments. TAS was influenced by infection with trematodes in Biomphlaria galabrata with S. mansoni (Jong-Brink and Oene 2005). B. alexandrina snails infected with S. mansoni showed a significant reduction in the levels of LPO and NO compared to uninfected snails, which may be due to developing schistosome larvae scavenging nutrients from the snail's hemolymph, resulting in a reduction in the amount of nutrients circulating to the nervous system (Habib et al. 2020). Additionally, Mossalem et al., (2018) reported a significant decrease in CAT and GSH and an increase of MDA in the tissues and hemolymph of B. alexandrina following infection with S. mansoni. However, B. truncatus with S. haematobium recorded a significant increase in the level of LPO and NO compared to uninfected snails at the shedding stage, which may be due to the different prepatent periods in the two species. Rizk et al., (2018) reported that B. alexandrina snails infected with S. mansoni and B. truncatus snails infected with S. haematobium demonstrated a high significant elevation in glutathione reductase (GR), catalase, and superoxide dismutase (SOD) activities. Changes were also reported in infected snail tissue homogenates (Koriem et al. 2016). The mentioned biochemical parameters were restored to their values in control uninfected snails upon treatment with sodium fluoride, suggesting its ability to inhibit oxidative stress and apoptosis produced in Schistosoma-infected snails (Koriem et al. 2016). In response to parasitic infection, B. alexandrina and B. truncatus snails increase their defensive haemocytes, which generate large volumes of ROS to damage or kill parasite larvae.

8.8 Impact of Schistosoma infection on 17β-esteradiol and testosterone hormones in tissues at 1st shedding stage..:

Steroid hormones testosterone and estradiol were promoted in Biomphalaria at shedding stage, while in Bulinus, they were suppressed. Steroid hormones have been reported in numerous molluscs, including B. alexandrina (Oehlmann and Schulte-Oehlmann, 2003; Croll and Wang, 2007; Omran, 2012; Ragheb et al., 2018)d truncatus (Dokmak et al., 2022). Hormonal reduction observed in Bulinus truncatus and increased in Biomphalaria alexandrina may contribute to fecundity loss in these infected snails (Ibrahim and Hussein, 2022). Steroid hormones are important for gonad development in snails (Alon et al., 2007). Hormone administration has been shown to stimulate spermatogenesis and oogenesis in molluscan species, including testosterone, estradiol, and progesterone in the gonads (Ibrahim and Abdel-Tawab, 2020; Hamdi et al., 2021; Sakr et al., 1992; Wang and Croll, 2004). Developing larvae can reduce gonad volumes and alter hormonal homeostasis, leading to inhibition of egg production (Bayne and Loker, 1987). Schistosomin, a peptide produced by the nervous system of infected snails following schistosome infection, interferes with the host's neuroendocrine system, inhibiting reproductive hormone action (De Jong-Brink, 1995).

8.9. Impact of Schistosoma infection on comet assay at 1st shedding stage.

The study found that infection with cercariae mansoni and haematobium caused a statistically significant increase in DNA fragmentation and migration in molluscan tissues compared to controls. This is consistent with other studies that have reported decreases in serotonin and dopamine concentrations in tissues during infection (Rizk et al., 2018), as well as DNA damage in Biomphalaria alexandrina homocytes (Mohamed, 2011) and hemocytes of infected Bulinus truncatus (Saad et al., 2013).

8.10. Impact of S. mansoni with B. alexandrina and S. haematobium with B. truncates on digestive and hermaphrodite gland at 1st shedding stage:

The study found severe damage to the cell constituents of the digestive and hermaphrodite glands of infected B. alexandrina and B. truncatus snails caused by trematode larvae. Changes in digestive glands and ovotestis induced by larval digenean trematode parasites have been reported to be dependent on the severity of infection, size, and types of larvae (Choubisa et al., 2012). Mechanical damages resulting from the migration, feeding, growth, and multiplication of trematode larvae, as well as physiological changes such as autolysis and/or necrosis, are possible explanations for these alterations. Previous studies have shown that redial stages cause more mechanical and physiological damage compared to sporocysts (Mohandas, 1977; Choubisa, 1988). Rediae engulf the host's digestive cells and utilize hydrolases for their extracellular digestion, contributing to physiological damages (Choubisa, 1988, 2008a ). It can be assumed that spore larval species observed within two host cell constituents' tissues in the digestive and hermaphrodite gland are more destructive for the two hosts. Parasitic secretions and excretory products that produce toxic effects may also be contributory factors (Erasmus, 1972).

The present study suggests that changes in the behavior of B. alexandrina and B. truncatus exposed to S. mansoni and S. haematobium, respectively, may be due to many interrelated factors, including disturbance in hormonal and biochemical components. Vector-parasite interaction-induced damage in DNA and disturbance in antioxidant systems may be responsible for hormone disorders in infected B. alexandrina and B. truncatus .

Acknowledgement

This research did not receive any specific grant from funding agencies in the public, commercial, or

not- for-profit sectors.

Conflict of interest. The authors declare that they have no competing interests.

This study was approved by Medical Malacology Department and received approval Scientific Ethics Committee by Theodor Bilharz Research Institute (TBRI), Imbaba, Giza, Egypt .

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Plates 1 and 2 are available in the Supplementary Files section

Plate1.png
Plate (1): impact of S. mansoni with B. alexandrina and S. haematobium with B. truncatus on comet assay parameters A- control B. alexandrina ; (B) B. alexandrina- infected ; C- control B. truncatus and. (D) infected B. truncatus at 1^st shedding stage .
Plate2.png
Plate (2): A, Light micrographs show the normal digestive glands and nomal hermaphrodite gland of B. alexanderina and& C normal digestive glands and nomal hermaphrodite gland of B. truncatus snails. Digestive cells (blue arrow), secretory cells (dark red arrow), Lumen (head dark red arrow) (H&E; x100; x200). Mature ovum (red arrow), Oocytes (black arrow), Sperms (yellow arrow). B & D show infected digestive and hermaphrodite gland where red arrow (s) spore capsule of cercariae species at1^st shedding stage.

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Impact of Schistosoma sp., infection on biological, behavioral, physiological, histological, and genotoxicological aspects of Biomphalaria alexandrina and Bulinus truncatus snails

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