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

Impact of Schistosoma sp., infection on biological, behavioral, physiological, histological, and genotoxicological aspects of Biomphalaria alexandrina and Bulinus truncatus snails | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article Impact of Schistosoma sp., infection on biological, behavioral, physiological, histological, and genotoxicological aspects of Biomphalaria alexandrina and Bulinus truncatus snails Heba Dokmak, olfat hamam, amina ibrahim This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-3110632/v1 This work is licensed under a CC BY 4.0 License Status: Published Journal Publication published 01 Feb, 2024 Read the published version in Acta Parasitologica → Version 1 posted 4 You are reading this latest preprint version Abstract 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 Figures Figure 1 Figure 2 Figure 3 Figure 4 Figure 5 Introduction 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. Materials and Methods 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 mm 2 . 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%. Results 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. truncat us. 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. alexandri na 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). Discussion 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 ). Conclusion 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 . Declarations 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 . References Abdel-Tawab, H, Ibrahim, AM, Hussein, T, Mohamed, F, (2022). 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Plates Plates 1 and 2 are available in the Supplementary Files section Supplementary Files 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. Cite Share Download PDF Status: Published Journal Publication published 01 Feb, 2024 Read the published version in Acta Parasitologica → Version 1 posted Reviewers agreed at journal 30 Aug, 2023 Reviewers invited by journal 19 Jul, 2023 Editor assigned by journal 02 Jul, 2023 First submitted to journal 27 Jun, 2023 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-3110632","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":219827489,"identity":"b3e803ef-8cf9-493a-a50e-1f82fb2701b1","order_by":0,"name":"Heba Dokmak","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAABA0lEQVRIiWNgGAWjYBACAwYeBgbGBiDrQAIzkEyQA4keeECKFmOwlgRStCSC2Az4tJiz9x788HPHNjm+48mHjW7UpKXPDzv8EGiLnZxuA3Ytlj3nkiV7z9w2ljzzLDk551hO7sbbaQZALcnGZgdwOOxGjoEEb9vtxA03cowP57BV5G6cnQDSciBxGy4t998Y//zbdrseouVfRbrh7PQP+LXc4DGTBtqSALTOODm3LSdBXjqHgC1n8tKsZdtuG84E+sU4ty/NcIN0TsGBBAM8fjl+9vDNt2235UEhJp3zLVlefnb65g8fKuzkcGnBYghYpQGxykFAvoEU1aNgFIyCUTASAACrym6xm53K3QAAAABJRU5ErkJggg==","orcid":"https://orcid.org/0000-0002-9856-1281","institution":"Theodor Bilharz Research Institute","correspondingAuthor":true,"submittingAuthor":false,"prefix":"","firstName":"Heba","middleName":"","lastName":"Dokmak","suffix":""},{"id":219827490,"identity":"64559860-07bc-4768-9a4b-26dcee583a3b","order_by":1,"name":"olfat hamam","email":"","orcid":"","institution":"Theodor Bilharz Research Institute","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"olfat","middleName":"","lastName":"hamam","suffix":""},{"id":219827491,"identity":"413883e8-706e-4743-a1b7-2798ccc6fb19","order_by":2,"name":"amina ibrahim","email":"","orcid":"","institution":"Theodor Bilharz Research Institute","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"amina","middleName":"","lastName":"ibrahim","suffix":""}],"badges":[],"createdAt":"2023-06-26 12:03:48","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-3110632/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-3110632/v1","draftVersion":[],"editorialEvents":[{"content":"https://doi.org/10.1007/s11686-023-00760-4","type":"published","date":"2024-02-01T15:01:36+00:00"}],"editorialNote":"","failedWorkflow":false,"files":[{"id":40535818,"identity":"0b0b89d2-33ad-4430-a69b-a890b76db0df","added_by":"auto","created_at":"2023-07-25 13:30:38","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":45213,"visible":true,"origin":"","legend":"\u003cp\u003eImpact of \u003cem\u003eS. mansoni\u003c/em\u003e with \u003cem\u003eB. alexandrina\u003c/em\u003eand \u003cem\u003eS. haematobium\u003c/em\u003e with \u003cem\u003eB. truncatus\u003c/em\u003e on infection rate (1-A), duration of shedding and pre-patent period (1-B), total cercarial production (1-C) and life span post miracidia species exposure (1-D) .\u003c/p\u003e","description":"","filename":"1.png","url":"https://assets-eu.researchsquare.com/files/rs-3110632/v1/4092f9e23cbb43e2869350fd.png"},{"id":40537031,"identity":"0094496f-0c24-4d49-9c07-531e5bad994a","added_by":"auto","created_at":"2023-07-25 13:38:38","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":359921,"visible":true,"origin":"","legend":"\u003cp\u003eImpact of \u003cem\u003eS. mansoni\u003c/em\u003e with \u003cem\u003eB. alexandrina\u003c/em\u003eand \u003cem\u003eS. haematobium\u003c/em\u003e with \u003cem\u003eB. truncatus\u003c/em\u003e on survival rate (2-A); on feeding behavior in \u003cem\u003eB\u003c/em\u003e. alexandrina (2-B), in \u003cem\u003eB\u003c/em\u003e. \u003cem\u003etruncatus\u003c/em\u003e (2-C), on fecundity in \u003cem\u003eB\u003c/em\u003e. alexandrina (2-D), in \u003cem\u003eB\u003c/em\u003e. \u003cem\u003etruncatus\u003c/em\u003e (2-E) and reproductive rate (2-F) in two infected snails.\u003c/p\u003e","description":"","filename":"2.png","url":"https://assets-eu.researchsquare.com/files/rs-3110632/v1/a2ef246d6465cc2d3fe534dd.png"},{"id":40535824,"identity":"ab01733b-fb87-4a0c-8b8b-3f60bd2caabd","added_by":"auto","created_at":"2023-07-25 13:30:38","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":585196,"visible":true,"origin":"","legend":"\u003cp\u003eImpact \u0026nbsp;\u0026nbsp;of \u003cem\u003eS. \u0026nbsp;mansoni\u003c/em\u003e with \u003cem\u003eB. alexandrina\u003c/em\u003e and \u003cem\u003eS. haematobium\u003c/em\u003e with \u003cem\u003eB. truncatus\u003c/em\u003e on total antioxidant (3-A), lipid peroxidase (3-B), nitrogen oxide (3-C), superoxide dismutase (3-D) and glutathione –s-transferase (3-E) at shedding stage.\u003c/p\u003e","description":"","filename":"3.png","url":"https://assets-eu.researchsquare.com/files/rs-3110632/v1/484c41a421034771528a8b6b.png"},{"id":40535823,"identity":"232b6de7-92d2-4713-89b1-152522e6e3c2","added_by":"auto","created_at":"2023-07-25 13:30:38","extension":"png","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":301726,"visible":true,"origin":"","legend":"\u003cp\u003eImpact \u0026nbsp;\u0026nbsp;of \u003cem\u003eS. mansoni\u003c/em\u003e \u0026nbsp;with \u003cem\u003eB. \u0026nbsp;alexandrina\u003c/em\u003e and \u003cem\u003eS. haematobium\u003c/em\u003e with \u003cem\u003eB. truncatus\u003c/em\u003e on 17β-esteradiol (4-A) and testosterone (4-B) in tissues at shedding stage.\u003c/p\u003e","description":"","filename":"4.png","url":"https://assets-eu.researchsquare.com/files/rs-3110632/v1/6d1ad9a765c749065a6da02c.png"},{"id":40537033,"identity":"79f6c1d2-f8ce-47c2-977d-74df66b07e3d","added_by":"auto","created_at":"2023-07-25 13:38:38","extension":"png","order_by":5,"title":"Figure 5","display":"","copyAsset":false,"role":"figure","size":10207,"visible":true,"origin":"","legend":"\u003cp\u003eImpact \u0026nbsp;\u0026nbsp;of \u003cem\u003eS. mansoni\u003c/em\u003e with \u003cem\u003eB. alexandrina\u003c/em\u003eand \u003cem\u003eS. haematobium\u003c/em\u003e with \u003cem\u003eB. truncatus\u003c/em\u003e on comet assay parameters.\u003c/p\u003e","description":"","filename":"5.png","url":"https://assets-eu.researchsquare.com/files/rs-3110632/v1/d675bf0cf2a7bcaf744266bd.png"},{"id":50674301,"identity":"fcdca2d5-7541-4f99-a7df-67d950a6fb73","added_by":"auto","created_at":"2024-02-05 15:10:10","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":747478,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-3110632/v1/5d3a7756-7d52-4ca1-b4cf-31dce2f72502.pdf"},{"id":40537032,"identity":"8a62c6e8-68e5-4955-a096-5b688bc965c6","added_by":"auto","created_at":"2023-07-25 13:38:38","extension":"png","order_by":1,"title":"","display":"","copyAsset":false,"role":"supplement","size":396132,"visible":true,"origin":"","legend":"\u003cp\u003ePlate (1): impact of \u003cem\u003eS\u003c/em\u003e. \u003cem\u003emansoni \u003c/em\u003ewith \u003cem\u003eB. alexandrina \u003c/em\u003eand \u003cem\u003eS\u003c/em\u003e. \u003cem\u003ehaematobium \u003c/em\u003ewith\u0026nbsp; \u003cem\u003eB. truncatus \u003c/em\u003eon comet assay parameters A- control\u003cem\u003e B. alexandrina\u003c/em\u003e ; \u003cem\u003e\u0026nbsp;\u003c/em\u003e(B) \u003cem\u003eB. alexandrina\u003c/em\u003e- infected \u003cem\u003e;\u003c/em\u003e C- control\u003cem\u003e B\u003c/em\u003e. \u003cem\u003etruncatus and. \u003c/em\u003e(D) infected \u003cem\u003eB\u003c/em\u003e. \u003cem\u003etruncatus \u003c/em\u003eat 1\u003csup\u003est\u003c/sup\u003e shedding stage .\u003c/p\u003e","description":"","filename":"Plate1.png","url":"https://assets-eu.researchsquare.com/files/rs-3110632/v1/fab5c57a908addf4b5f04272.png"},{"id":40535820,"identity":"3e34e18a-6cdd-45b3-9638-2ec4710271ce","added_by":"auto","created_at":"2023-07-25 13:30:38","extension":"png","order_by":2,"title":"","display":"","copyAsset":false,"role":"supplement","size":495259,"visible":true,"origin":"","legend":"\u003cp\u003ePlate (2): A, Light micrographs show the normal digestive glands and nomal hermaphrodite gland of \u003cem\u003eB. alexanderina \u003c/em\u003eand\u0026amp; C\u003cem\u003e \u003c/em\u003enormal digestive glands and nomal hermaphrodite gland\u003cem\u003e \u003c/em\u003eof \u003cem\u003eB. truncatus \u003c/em\u003esnails. Digestive \u0026nbsp;\u0026nbsp;cells (blue arrow), secretory\u0026nbsp;\u0026nbsp; cells (dark red arrow), \u0026nbsp;Lumen (head dark\u0026nbsp; \u0026nbsp;red arrow) (H\u0026amp;E; x100; x200). \u0026nbsp;Mature ovum (red arrow), \u0026nbsp;Oocytes (black arrow), \u0026nbsp;\u0026nbsp;Sperms (yellow arrow).\u0026nbsp; B \u0026amp; D show infected digestive and hermaphrodite gland where red arrow\u0026nbsp;\u0026nbsp; (s) spore capsule of cercariae species\u0026nbsp;\u0026nbsp; at1\u003csup\u003est\u003c/sup\u003e shedding stage.\u003c/p\u003e","description":"","filename":"Plate2.png","url":"https://assets-eu.researchsquare.com/files/rs-3110632/v1/db6ccbde2c6b5638b89d48cf.png"}],"financialInterests":"","formattedTitle":"Impact of Schistosoma sp., infection on biological, behavioral, physiological, histological, and genotoxicological aspects of Biomphalaria alexandrina and Bulinus truncatus snails","fulltext":[{"header":"Introduction","content":"\u003cp\u003eSchistosomiasis is a chronic parasitic disease caused by trematodes of the genus \u003cem\u003eSchistosoma\u003c/em\u003e, and it is considered the second most devastating disease in terms of morbidity and mortality worldwide (Ibrahim et al., \u003cspan class=\"CitationRef\"\u003e2023b\u003c/span\u003e; WHO \u003cspan class=\"CitationRef\"\u003e2023\u003c/span\u003e). This disease is prevalent in tropical and subtropical areas, affecting approximately 240\u0026nbsp;million people worldwide, with about 700\u0026nbsp;million people at risk, especially in poor communities with inadequate sanitation facilities (WHO \u003cspan class=\"CitationRef\"\u003e2022\u003c/span\u003e; Ibrahim et al. \u003cspan class=\"CitationRef\"\u003e2023a\u003c/span\u003e) (WHO 2001, 2011, 2013, and 2012\u0026ndash;2020) and (Obare et al., \u003cspan class=\"CitationRef\"\u003e2016\u003c/span\u003e). \u003cem\u003eSchistosoma mansoni\u003c/em\u003e and \u003cem\u003eS. haematobium\u003c/em\u003e are the two parasites that cause the most widespread forms of intestinal and urogenital schistosomiasis (Mansour and Ibrahim \u003cspan class=\"CitationRef\"\u003e2023\u003c/span\u003e). In our laboratory, we use the infection of \u003cem\u003eB. alexandrina\u003c/em\u003e with \u003cem\u003eS. mansoni\u003c/em\u003e and \u003cem\u003eB. truncatus\u003c/em\u003e with \u003cem\u003eS. haematobium\u003c/em\u003e 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 \u003cem\u003eB. alexandrina\u003c/em\u003e becomes infected with \u003cem\u003eS. mansoni\u003c/em\u003e and \u003cem\u003eB. truncatus\u003c/em\u003e becomes infected with \u003cem\u003eS. haematobium\u003c/em\u003e, the development of the hermaphroditic reproductive system of the two snail species is severely retarded (Joosse and Van 1986, McClelland and Bourns \u003cspan class=\"CitationRef\"\u003e1969\u003c/span\u003e, and Sluiters et al. \u003cspan class=\"CitationRef\"\u003e1980\u003c/span\u003e), 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 \u003cspan class=\"CitationRef\"\u003e1969\u003c/span\u003e, Curtis \u003cspan class=\"CitationRef\"\u003e1990\u003c/span\u003e, \u003cspan class=\"CitationRef\"\u003e1993\u003c/span\u003e, Levri and Lively \u003cspan class=\"CitationRef\"\u003e1996\u003c/span\u003e). 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 \u003cspan class=\"CitationRef\"\u003e1985\u003c/span\u003e, Hurd \u003cspan class=\"CitationRef\"\u003e1990\u003c/span\u003e). 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. \u003cspan class=\"CitationRef\"\u003e2001\u003c/span\u003e) (Ibrahim et al. \u003cspan class=\"CitationRef\"\u003e2018\u003c/span\u003e; Morad et al. \u003cspan class=\"CitationRef\"\u003e2022\u003c/span\u003e). Gastropod snails have been reported to be vectors of certain larval digeneans (Choubisa and Sharma \u003cspan class=\"CitationRef\"\u003e1986\u003c/span\u003e; Abdel-Tawab et al. \u003cspan class=\"CitationRef\"\u003e2022\u003c/span\u003e). 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 \u003cspan class=\"CitationRef\"\u003e1985\u003c/span\u003e; Soomro et al. \u003cspan class=\"CitationRef\"\u003e2005\u003c/span\u003e; Huffman et al. \u003cspan class=\"CitationRef\"\u003e2009\u003c/span\u003e; Abdel-Tawab et al. \u003cspan class=\"CitationRef\"\u003e2022\u003c/span\u003e; Morad et al. \u003cspan class=\"CitationRef\"\u003e2022\u003c/span\u003e). 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 \u003cem\u003eB. alexandrina-S. mansoni\u003c/em\u003e and \u003cem\u003eB. truncatus-S. haematobium\u003c/em\u003e models. Biochemical, histopathological, and genotoxic parameters were measured in homogenate tissue of both infected snails and compared to uninfected snails.\u003c/p\u003e\n"},{"header":"Materials and Methods","content":"\u003cp\u003e\u003cstrong\u003e2.2.\u003c/strong\u003e Species snails with infections:\u003c/p\u003e\n\u003cdiv class=\"BlockQuote\"\u003e\n\u003cp\u003eJuvenile specimens of both \u003cem\u003eB. alexandrina\u003c/em\u003e (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 \u003cem\u003eB. alexandrina\u003c/em\u003e snails were individually exposed to 5\u0026ndash;8 freshly hatched \u003cem\u003eS. mansoni\u003c/em\u003e miracidia, and triplicate groups of 10 \u003cem\u003eB. truncatus\u003c/em\u003e snails were individually exposed to 8\u0026ndash;15 freshly hatched \u003cem\u003eS. haematobium\u003c/em\u003e miracidia for 3 hours at 25\u0026deg;C in 2 ml vials containing dechlorinated tap water, according to the protocol described by Sluiters et al. (\u003cspan class=\"CitationRef\"\u003e1980\u003c/span\u003e) Miracidia of \u003cem\u003eS. mansoni\u003c/em\u003e and \u003cem\u003eS. haematobium\u003c/em\u003e 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 \u003cem\u003eB. alexandrina\u003c/em\u003e and eight weeks after infection with \u003cem\u003eB. truncatus.\u003c/em\u003e The infection rate was calculated in \u003cem\u003eB. alexandrina\u003c/em\u003e four weeks after infection and in \u003cem\u003eB. truncatus\u003c/em\u003e eight weeks after infection, following the method by Coles (\u003cspan class=\"CitationRef\"\u003e1973\u003c/span\u003e): 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 (\u003cspan class=\"CitationRef\"\u003e1963\u003c/span\u003e) by the following equation: survival rate = \u003cspan class=\"InlineEquation\"\u003e\u003cspan class=\"mathinline\"\u003e\\(\\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\\)\u003c/span\u003e\u003c/span\u003e 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., (\u003cspan class=\"CitationRef\"\u003e1995\u003c/span\u003e).\u003c/p\u003e\n\u003c/div\u003e\n\u003cp\u003e\u003cstrong\u003e2.3.\u003c/strong\u003e Feeding behavior:\u003c/p\u003e\n\u003cp\u003eAbout 10 snails of the same size (8-9mm) from each species infected and control groups were housed in a plastic container (16 \u0026times; 23 \u0026times; 9 cm) and provided with 50 circle of washed clean fresh lettuce leaves measuring 4 mm\u003csup\u003e2\u003c/sup\u003e. The snails' were starved before the experiment for one day and then the food was given (Valarmathi \u003cspan class=\"CitationRef\"\u003e2017\u003c/span\u003e). 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., \u003cspan class=\"CitationRef\"\u003e2021\u003c/span\u003e). Trireplicate of each species group were done and assessed side by side with the control ones.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003e2.4.\u003c/strong\u003e Biological parameters:\u003c/p\u003e\n\u003cp\u003eTo examine the fecundity of the two snail species, pieces of Styrofoam sheets (5 \u0026times; 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. (\u003cspan class=\"CitationRef\"\u003e2004\u003c/span\u003e).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003e3.\u003c/strong\u003e Species snail tissue homogenates and biochemical estimations:\u003c/p\u003e\n\u003cp\u003eTo 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\u0026deg;C. The supernatants were used for different biochemical analyses. Biodiagnostic kits (Biodiagnostic Dokki, Giza, Egypt) were used to determine SOD (Damerval et al., \u003cspan class=\"CitationRef\"\u003e1986\u003c/span\u003e) and GST (Beutler \u003cspan class=\"CitationRef\"\u003e1963\u003c/span\u003e) levels. Tissue malondialdehyde (lipid peroxide) was assessed according to Ohkawa et al. (\u003cspan class=\"CitationRef\"\u003e1979\u003c/span\u003e). 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 (\u003cspan class=\"CitationRef\"\u003e1962\u003c/span\u003e), and total antioxidant capacity was estimated using a kit (Cat. No. TA 2513) according to Koracevic et al. (\u003cspan class=\"CitationRef\"\u003e2001\u003c/span\u003e).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003e3.1.\u003c/strong\u003e Steroid sex hormones (testosterone and 17\u0026beta;-estradiol)\u003c/p\u003e\n\u003cp\u003eThe levels of steroid hormones, specifically testosterone and 17\u0026beta;-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., \u003cspan class=\"CitationRef\"\u003e2023\u003c/span\u003e).\u003c/p\u003e\n\u003cp\u003e3.2. Genotoxicity by Comet assay:\u003c/p\u003e\n\u003cp\u003eSpecies snail (7\u0026ndash;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.. (\u003cspan class=\"CitationRef\"\u003e1988\u003c/span\u003e) and Grazeffe et al., (\u003cspan class=\"CitationRef\"\u003e2008\u003c/span\u003e).\u003c/p\u003e\n\u003cp\u003e3.3. Histopathological alterations:\u003c/p\u003e\n\u003cp\u003eSimultaneous positive infection of \u003cem\u003eB. alexandrina\u003c/em\u003e with \u003cem\u003eS. mansoni\u003c/em\u003e and \u003cem\u003eB. truncatus\u003c/em\u003e with \u003cem\u003eS. haematobium\u003c/em\u003e 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\u0026ndash;8\u0026micro;m) were then stained with haematoxylin and eosin, following the protocol by Mohamed and Saad (\u003cspan class=\"CitationRef\"\u003e1990\u003c/span\u003e). Similarly, sections of the control snails' digestive and hermaphrodite glands were also prepared.\u003c/p\u003e\n\u003cp\u003e3.4. Statistical analysis:\u003c/p\u003e\n\u003cp\u003eThe values of biological and biochemical parameters were expressed as mean\u0026thinsp;\u0026plusmn;\u0026thinsp;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\u0026thinsp;\u0026lt;\u0026thinsp;0.05, corresponding to a confidence level of 95%.\u003c/p\u003e\n"},{"header":"Results","content":"\u003cp\u003e4.1. Snail\u0026rsquo;s infection rate:\u003c/p\u003e\n\u003cp\u003eInfection rate in \u003cem\u003eB. alexandrina\u003c/em\u003e with \u003cem\u003eS. mansoni\u003c/em\u003e was recorded 34.7% (Fig.\u0026nbsp;1-A) while recorded 30.4% in \u003cem\u003eB.truncatus\u003c/em\u003e with \u003cem\u003eS. haematobium\u003c/em\u003e.\u003c/p\u003e\n\u003cp\u003e4.2. Snail\u0026rsquo;s duration of shedding and prepatent period:\u003c/p\u003e\n\u003cp\u003eDuration of shedding varied from 21 to 37 days (Mean: 23.8\u0026thinsp;\u0026plusmn;\u0026thinsp;5.5) in \u003cem\u003eB. alexandrina\u003c/em\u003e and from 18 to 40 days (Mean: 24.6\u0026thinsp;\u0026plusmn;\u0026thinsp;2.6) for \u003cem\u003eB. truncat\u003c/em\u003eus. Prepatent period was 32 days post-infection for \u003cem\u003eB. alexandrina\u003c/em\u003e and 46 days post-infection for \u003cem\u003eB. truncatus\u003c/em\u003e (see Fig.\u0026nbsp;1-B).\u003c/p\u003e\n\u003cp\u003e4.3. Mean total number of cercariae per snails:\u003c/p\u003e\n\u003cp\u003eThe mean number of crecariae per snail Fig.\u0026nbsp;(1-C) in \u003cem\u003eB. alexandri\u003c/em\u003ena was 2297.4\u0026thinsp;\u0026plusmn;\u0026thinsp;272.5 (p\u0026thinsp;\u0026lt;\u0026thinsp;0.01) and recorded 1637.3\u0026thinsp;\u0026plusmn;\u0026thinsp;307.5) (p\u0026thinsp;\u0026lt;\u0026thinsp;0.01) in positive \u003cem\u003eB. truncatus\u003c/em\u003e .\u003c/p\u003e\n\u003cp\u003e4.4. Snail\u0026rsquo;s mean life span:\u003c/p\u003e\n\u003cp\u003eIt is worth mentioning that the mean lifespan was recorded as 57.0\u0026thinsp;\u0026plusmn;\u0026thinsp;1.21 days in \u003cem\u003eB. alexandrina\u003c/em\u003e (see Fig.\u0026nbsp;1-D) and 65.9\u0026thinsp;\u0026plusmn;\u0026thinsp;1.6 days in \u003cem\u003eB. truncates\u003c/em\u003e.\u003c/p\u003e\n\u003cp\u003e4.5. Snail\u0026rsquo;s survival rate at first shedding:\u003c/p\u003e\n\u003cp\u003eThe survival rate of \u003cem\u003eB. alexandrina\u003c/em\u003e exposed to \u003cem\u003eSchistosoma mansoni\u003c/em\u003e at first cercarial shedding was 65.2%, while the survival rate of \u003cem\u003eB. truncatus\u003c/em\u003e exposed to \u003cem\u003eS. haematobium\u003c/em\u003e was 56.4%, as compared to the survival rate in the respective control groups (refer to Fig.\u0026nbsp;2-A).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003e4.6.\u003c/strong\u003e Impact of \u003cem\u003eSchistosoma mansoni\u003c/em\u003e with \u003cem\u003eBiomphlaria alexandrina\u003c/em\u003e and \u003cem\u003eS haematobium\u003c/em\u003e with \u003cem\u003eBulinus truncatus\u003c/em\u003e on feeding behaviour, fecundity and reproductive rate.\u003c/p\u003e\n\u003cp\u003eDuring the prepatent period, the number of feeding \u003cem\u003eB. alexandrina\u003c/em\u003e 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.\u0026nbsp;2-B). The same pattern was observed in \u003cem\u003eB. truncatus\u003c/em\u003e infected with \u003cem\u003eS. haematobium\u003c/em\u003e (Fig.\u0026nbsp;2-C). Additionally, the fecundity of \u003cem\u003eB. alexandrina\u003c/em\u003e showed a pattern of ceasing egg-laying for 4 weeks during the prepatent period (see Fig.\u0026nbsp;2-D), which was also observed in \u003cem\u003eB. truncatus\u003c/em\u003e after being exposed to miracidia for 7 weeks(see Fig.\u0026nbsp;2-E). The net reproductive rate (Ro) in infected \u003cem\u003eB. alexandrina\u003c/em\u003e and \u003cem\u003eB. truncatus\u003c/em\u003e was significantly reduced to 47.7% and 84.6% of its value in the respective control groups (refer to Fig.\u0026nbsp;2-F).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003e5.\u003c/strong\u003e Impact of infection with \u003cem\u003eSchistosoma mansoni\u003c/em\u003e in \u003cem\u003eBiomphlaria alexandrina\u003c/em\u003e and infection with \u003cem\u003eS haematobium\u003c/em\u003e in \u003cem\u003eBulinus truncatus\u003c/em\u003e on oxidative stress paremeters at 1st shedding stage.\u003c/p\u003e\n\u003cp\u003e\u003cem\u003eSchistosomiasis mansoni\u003c/em\u003e and \u003cem\u003eS. haematobium\u003c/em\u003e infection impacted the levels of TAO, LPO, NO, SOD, and GST in the homogenized tissue of infected \u003cem\u003eB. alexandrina\u003c/em\u003e and \u003cem\u003eB. truncatus\u003c/em\u003e at the shedding stage. TAO activity showed a significantly higher value (p\u0026thinsp;\u0026lt;\u0026thinsp;0.05) post 32 days of infection in the homogenized tissue of \u003cem\u003eB. alexandrina\u003c/em\u003e as compared to the uninfected group, and the same result was recorded post 46 days of infection in infected \u003cem\u003eB. truncatus\u003c/em\u003e snails (refer to Fig.\u0026nbsp;3-A). This suggests that the infections were stressful for the snails. Lipid peroxidation (LPO) activity showed a significant reduction in infected \u003cem\u003eB. alexandrina\u003c/em\u003e snails relative to the value in uninfected snails, while in \u003cem\u003eB. truncatus\u003c/em\u003e snails, LPO activity increased significantly compared to the control group (refer to Fig.\u0026nbsp;3-B). Meanwhile, a significant elevation in the levels of NO was observed in tissue homogenate of \u003cem\u003eB. truncatus\u003c/em\u003e snails post 46 days of infection, while the level of NO in infected \u003cem\u003eB. alexandrina\u003c/em\u003e snails recorded a significant reduction post 32 days of infection as compared to the uninfected group of snails (refer to Fig.\u0026nbsp;3C). Superoxide dismutase (SOD) levels in infected \u003cem\u003eB. alexandrina\u003c/em\u003e and \u003cem\u003eB. truncatus\u003c/em\u003e snails were higher than those in uninfected snails in both species (refer to Fig.\u0026nbsp;3-D). The highest Glutathione-s-transferase (GST) value was measured in infected \u003cem\u003eB. truncatus\u003c/em\u003e snails post 46 days of infection, while \u003cem\u003eB. alexandrina\u003c/em\u003e snails post 32 days of infection revealed a reduction compared to uninfected \u003cem\u003eB. alexandrina\u003c/em\u003e snails (refer to Fig.\u0026nbsp;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 \u003cem\u003eB. truncatus\u003c/em\u003e (46 days) as compared to \u003cem\u003eB. alexandrina\u003c/em\u003e (32 days), regardless of the parasite species.\u003c/p\u003e\n\u003cp\u003e\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003e5.1.\u003c/strong\u003e Impact of \u003cem\u003eS. mansoni\u003c/em\u003e with \u003cem\u003eB. alexandrina\u003c/em\u003e and \u003cem\u003eS. haematobium\u003c/em\u003e with \u003cem\u003eB. truncatus\u003c/em\u003e on 17\u0026beta;-esteradiol and testosterone hormones in tissues at 1st shedding stage.\u003c/p\u003e\n\u003cp\u003eIn infected \u003cem\u003eB. alexandrina\u003c/em\u003e snails, the production of cercariae resulted in significant increases in the concentration of 17\u0026beta;-estradiol and testosterone in homogenized tissues at 32 days post-infection (refer to Fig.\u0026nbsp;4-A), while in infected \u003cem\u003eB. truncatus\u003c/em\u003e snails, there was a significant reduction in the concentration of 17\u0026beta;-estradiol and testosterone hormones post 46 days post-infection compared to their concentration in non-infected control snails (p\u0026thinsp;\u0026lt;\u0026thinsp;0.05) (refer to Fig.\u0026nbsp;4-B).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003e6.\u003c/strong\u003e Impact of \u003cem\u003eS. mansoni\u003c/em\u003e with \u003cem\u003eB\u003c/em\u003e. \u003cem\u003ealexandrina\u003c/em\u003e and \u003cem\u003eS. haematobium\u003c/em\u003e with \u003cem\u003eB. truncatus\u003c/em\u003e on comet assay at 1st shedding stage.\u003c/p\u003e\n\u003cp\u003eThe comet assay was used to monitor DNA damage in \u003cem\u003eB. alexandrina\u003c/em\u003e and \u003cem\u003eB. truncatus\u003c/em\u003e snails infected with \u003cem\u003eSchistosoma mansoni\u003c/em\u003e and \u003cem\u003eS. haematobium\u003c/em\u003e, respectively. Tailed % and tailed length, which indicate cell malformation, showed significant increases in infected \u003cem\u003eB. alexandrina\u003c/em\u003e snails as compared to uninfected groups (refer to Fig.\u0026nbsp;5 \u0026amp; plate 1). Meanwhile, the normal % DNA in the tail that migrated from the head increased in infected \u003cem\u003eB. alexandrina\u003c/em\u003e 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.\u0026nbsp;5\u0026amp; plate 1). Olive tail moment, which indicates DNA fragmentation, was significantly increased in infected \u003cem\u003eB. alexandrina\u003c/em\u003e snails as compared to the control group (p\u0026thinsp;\u0026lt;\u0026thinsp;0.05). The same negative impact on comet assay parameters was observed in infected \u003cem\u003eB. truncatus\u003c/em\u003e snails with S. haematobium at the shedding stage (refer to Fig.\u0026nbsp;5 \u0026amp; plate 1).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003e7.\u003c/strong\u003e Impact of \u003cem\u003eS. mansoni\u003c/em\u003e with \u003cem\u003eB\u003c/em\u003e. \u003cem\u003ealexandrina\u003c/em\u003e and \u003cem\u003eS. haematobium\u003c/em\u003e with \u003cem\u003eB. truncatus\u003c/em\u003e on the snails\u0026rsquo; digestive and hermaphrodite glands histology at shedding stage.\u003c/p\u003e\n\u003cp\u003eInfection of \u003cem\u003eB. alexandrina\u003c/em\u003e and \u003cem\u003eB. truncatus\u003c/em\u003e snails with \u003cem\u003eS. mansoni\u003c/em\u003e and \u003cem\u003eS. haematobium\u003c/em\u003e, 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 \u0026amp; 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 \u0026amp; 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 \u0026amp; 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 \u0026amp; D).\u003c/p\u003e"},{"header":"Discussion","content":"\u003cp\u003e8.1.Snail\u0026rsquo;s infection rate:\u003c/p\u003e\n\u003cp\u003eLab observations of \u003cem\u003eB. alexandrina\u003c/em\u003e with \u003cem\u003eS. mansoni\u003c/em\u003e and \u003cem\u003eB. truncatus\u003c/em\u003e with \u003cem\u003eS. haematobium\u003c/em\u003e agreed with Makanga's (1981) finding of 30% IR in young \u003cem\u003eB. pfeifferi\u003c/em\u003e with \u003cem\u003eS. mansoni\u003c/em\u003e, but differed from Southgate et al., (\u003cspan class=\"CitationRef\"\u003e2000\u003c/span\u003e) and Ibikounl\u0026eacute; et al., (\u003cspan class=\"CitationRef\"\u003e2012\u003c/span\u003e) who reported higher IR in \u003cem\u003eB. pfeifferi\u003c/em\u003e with \u003cem\u003eS. mansoni\u003c/em\u003e. \u003cem\u003eB. truncatus\u003c/em\u003e 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 \u003cem\u003eet al.\u003c/em\u003e, 1953).\u003c/p\u003e\n\u003cp\u003e8.2. Snail\u0026rsquo;s duration of shedding and prepatent period:\u003c/p\u003e\n\u003cp\u003eThe mean prepatent period for \u003cem\u003eB. alexandrina\u003c/em\u003e and \u003cem\u003eB. truncatus\u003c/em\u003e corresponded to Kechemir and Combes' 1982 findings of 41\u0026ndash;56 days and; Pfl\u0026uuml;ger et al., \u003cspan class=\"CitationRef\"\u003e1984\u003c/span\u003e.\u003c/p\u003e\n\u003cp\u003e8.3. Mean total number of cercariae per snails:\u003c/p\u003e\n\u003cp\u003eThe total number of cercariae/snail counted in this study was different than that reported by Kechemir and Combes (\u003cspan class=\"CitationRef\"\u003e1982\u003c/span\u003e) and Kechemir (\u003cspan class=\"CitationRef\"\u003e1985\u003c/span\u003e) in \u003cem\u003eB. glabrata\u003c/em\u003e. It also concords with those reported in \u003cem\u003eBulinus truncatus\u003c/em\u003e infected by miracidia (from 29 to 65 days at 24\u0026ndash;26\u0026deg;C: Lo 1972; Kechemir and Combes \u003cspan class=\"CitationRef\"\u003e1982\u003c/span\u003e; Pfl\u0026uuml;ger et al., \u003cspan class=\"CitationRef\"\u003e1984\u003c/span\u003e). 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., \u003cspan class=\"CitationRef\"\u003e2018\u003c/span\u003e).\u003c/p\u003e\n\u003cp\u003e8.4. Snail\u0026rsquo;s mean life span:\u003c/p\u003e\n\u003cp\u003eThe life-span of cercaria-positive snails was 45\u0026ndash;81 days (mean: 57.0\u0026thinsp;\u0026plusmn;\u0026thinsp;1.2) for \u003cem\u003eB. alexandrina\u003c/em\u003e and 55\u0026ndash;91 days (mean: 65.9\u0026thinsp;\u0026plusmn;\u0026thinsp;1.6) for \u003cem\u003eB. truncatus\u003c/em\u003e. Archibald (\u003cspan class=\"CitationRef\"\u003e1933\u003c/span\u003e) reported a cercaria-positive \u003cem\u003eB. truncatus\u003c/em\u003e 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., \u003cspan class=\"CitationRef\"\u003e2010\u003c/span\u003e).\u003c/p\u003e\n\u003cp\u003eCurrently, 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., \u003cspan class=\"CitationRef\"\u003e2020\u003c/span\u003e).\u003c/p\u003e\n\u003cp\u003e8.5. Snail\u0026rsquo;s survival rate at 1st shedding stage:\u003c/p\u003e\n\u003cp\u003eThis study reported a reduction in the survival rate of two snail species upon shedding cercariae, which agrees with Mangal et al., (\u003cspan class=\"CitationRef\"\u003e2010\u003c/span\u003e) who observed lower survival rates in snails exposed to \u003cem\u003eS. mansoni\u003c/em\u003e 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., \u003cspan class=\"CitationRef\"\u003e1982\u003c/span\u003e). Woolhouse (\u003cspan class=\"CitationRef\"\u003e1989\u003c/span\u003e) found that patent infections of \u003cem\u003eS. species\u003c/em\u003e increased per capita mortality rates of \u003cem\u003eBulinus globosus\u003c/em\u003e and \u003cem\u003eB. pfeifferia\u003c/em\u003e, 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, \u003cspan class=\"CitationRef\"\u003e1980\u003c/span\u003e) 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., \u003cspan class=\"CitationRef\"\u003e1999\u003c/span\u003e).\u003c/p\u003e\n\u003cp\u003e8.6. Impact of \u003cem\u003eSchistosoma\u003c/em\u003e infection on feeding behaviour, fecundity and reproductive rate:\u003c/p\u003e\n\u003cp\u003eInfected \u003cem\u003eB. alexandrina\u003c/em\u003e and \u003cem\u003eB. truncatus\u003c/em\u003e tended to feed more frequently than uninfected snails. This agrees with Shinagawa et al., (\u003cspan class=\"CitationRef\"\u003e2001\u003c/span\u003e) 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, \u003cspan class=\"CitationRef\"\u003e2002\u003c/span\u003e; Poulin, \u003cspan class=\"CitationRef\"\u003e2010\u003c/span\u003e; Thomas, Adamo, \u0026amp; Moore, \u003cspan class=\"CitationRef\"\u003e2005\u003c/span\u003e). 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 \u003cspan class=\"CitationRef\"\u003e1985\u003c/span\u003e, Hurd \u003cspan class=\"CitationRef\"\u003e1990\u003c/span\u003e). 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, \u003cspan class=\"CitationRef\"\u003e2006\u003c/span\u003e; Lafferty and Kuris, \u003cspan class=\"CitationRef\"\u003e2009\u003c/span\u003e). 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, \u003cspan class=\"CitationRef\"\u003e1974\u003c/span\u003e; Choubisa, \u003cspan class=\"CitationRef\"\u003e1988\u003c/span\u003e). Infection with \u003cem\u003eS. mansoni\u003c/em\u003e or \u003cem\u003eS. haematobium\u003c/em\u003e miracidia caused \u003cem\u003eB. alexandrina\u003c/em\u003e and \u003cem\u003eB. truncatus\u003c/em\u003e snails to cease egg-laying post-exposure, resulting in a reduction in reproduction (Joosse and Van 1986, McClelland et al. 1996, Sluiters et al. \u003cspan class=\"CitationRef\"\u003e1980\u003c/span\u003e). The development of the hermaphrodite reproductive system of \u003cem\u003eL. stagnalis\u003c/em\u003e infected with \u003cem\u003eT. ocellata\u003c/em\u003e was severely retarded, resulting in almost no eggs being produced (Joosse and Van 1986, McClelland et al., 1996, Sluiters et al. \u003cspan class=\"CitationRef\"\u003e1980\u003c/span\u003e, Thornhill et al. \u003cspan class=\"CitationRef\"\u003e1986\u003c/span\u003e). Reductions in fecundity were also observed in three \u003cem\u003eBulinus\u003c/em\u003e species infected with \u003cem\u003eS. haematobium\u003c/em\u003e (Fryer et al. \u003cspan class=\"CitationRef\"\u003e1990\u003c/span\u003e). 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 \u003cspan class=\"CitationRef\"\u003e1949\u003c/span\u003e, McClelland and Bourns \u003cspan class=\"CitationRef\"\u003e1969\u003c/span\u003e, Meier and Meier-Brook \u003cspan class=\"CitationRef\"\u003e1981\u003c/span\u003e, Alberto-silva et al. \u003cspan class=\"CitationRef\"\u003e2015\u003c/span\u003e). 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 (\u003cspan class=\"CitationRef\"\u003e1981\u003c/span\u003e), 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 \u003cspan class=\"CitationRef\"\u003e1949\u003c/span\u003e, McClelland and Bourns \u003cspan class=\"CitationRef\"\u003e1969\u003c/span\u003e). 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 \u003cspan class=\"CitationRef\"\u003e1979\u003c/span\u003e). 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.\u003c/p\u003e\n\u003cp\u003e8.7. Impact of \u003cem\u003eSchistosoma\u003c/em\u003e infection on oxidative stress paremeters at 1st shedding stage.\u003c/p\u003e\n\u003cp\u003eIncreasing the level of TAO in infected \u003cem\u003eB. alexandrina\u003c/em\u003e and \u003cem\u003eB. truncatus\u003c/em\u003e 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 \u003cspan class=\"CitationRef\"\u003e2006\u003c/span\u003e, Saboor-yaraghi et al., \u003cspan class=\"CitationRef\"\u003e2011\u003c/span\u003e, Hadas\u0026acute; and Stankiewicz 1996, Mone et al. \u003cspan class=\"CitationRef\"\u003e2011\u003c/span\u003e). Gornowicz et al. (\u003cspan class=\"CitationRef\"\u003e2013\u003c/span\u003e) found significant differences in TAS between control and \u003cem\u003eP. elegans\u003c/em\u003e-infected \u003cem\u003eLymnaea stagnalis\u003c/em\u003e during the initial period of the experiments. TAS was influenced by infection with trematodes in \u003cem\u003eBiomphlaria galabrata\u003c/em\u003e with \u003cem\u003eS. mansoni\u003c/em\u003e (Jong-Brink and Oene \u003cspan class=\"CitationRef\"\u003e2005\u003c/span\u003e). \u003cem\u003eB. alexandrina\u003c/em\u003e snails infected with \u003cem\u003eS. mansoni\u003c/em\u003e showed a significant reduction in the levels of LPO and NO compared to uninfected snails, which may be due to developing \u003cem\u003eschistosome\u003c/em\u003e 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. \u003cspan class=\"CitationRef\"\u003e2020\u003c/span\u003e). Additionally, Mossalem et al., (\u003cspan class=\"CitationRef\"\u003e2018\u003c/span\u003e) reported a significant decrease in CAT and GSH and an increase of MDA in the tissues and hemolymph of \u003cem\u003eB. alexandrina\u003c/em\u003e following infection with \u003cem\u003eS. mansoni\u003c/em\u003e. However, \u003cem\u003eB. truncatus\u003c/em\u003e with \u003cem\u003eS. haematobium\u003c/em\u003e 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., (\u003cspan class=\"CitationRef\"\u003e2018\u003c/span\u003e) reported that \u003cem\u003eB. alexandrina\u003c/em\u003e snails infected with \u003cem\u003eS. mansoni\u003c/em\u003e and \u003cem\u003eB. truncatus\u003c/em\u003e snails infected with \u003cem\u003eS. haematobium\u003c/em\u003e 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. \u003cspan class=\"CitationRef\"\u003e2016\u003c/span\u003e). 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 \u003cem\u003eSchistosoma\u003c/em\u003e-infected snails (Koriem et al. \u003cspan class=\"CitationRef\"\u003e2016\u003c/span\u003e). In response to parasitic infection, \u003cem\u003eB. alexandrina\u003c/em\u003e and \u003cem\u003eB. truncatus\u003c/em\u003e snails increase their defensive haemocytes, which generate large volumes of ROS to damage or kill parasite larvae.\u003c/p\u003e\n\u003cp\u003e8.8 Impact of \u003cem\u003eSchistosoma\u003c/em\u003e infection on 17\u0026beta;-esteradiol and testosterone hormones in tissues at 1st shedding stage..:\u003c/p\u003e\n\u003cp\u003eSteroid hormones testosterone and estradiol were promoted in \u003cem\u003eBiomphalaria\u003c/em\u003e at shedding stage, while in \u003cem\u003eBulinus\u003c/em\u003e, they were suppressed. Steroid hormones have been reported in numerous molluscs, including \u003cem\u003eB. alexandrina\u003c/em\u003e (Oehlmann and Schulte-Oehlmann, \u003cspan class=\"CitationRef\"\u003e2003\u003c/span\u003e; Croll and Wang, \u003cspan class=\"CitationRef\"\u003e2007\u003c/span\u003e; Omran, \u003cspan class=\"CitationRef\"\u003e2012\u003c/span\u003e; Ragheb et al., \u003cspan class=\"CitationRef\"\u003e2018\u003c/span\u003e)d \u003cem\u003etruncatus\u003c/em\u003e (Dokmak et al., 2022). Hormonal reduction observed in \u003cem\u003eBulinus truncatus\u003c/em\u003e and increased in \u003cem\u003eBiomphalaria alexandrina\u003c/em\u003e may contribute to fecundity loss in these infected snails (Ibrahim and Hussein, \u003cspan class=\"CitationRef\"\u003e2022\u003c/span\u003e). Steroid hormones are important for gonad development in snails (Alon et al., \u003cspan class=\"CitationRef\"\u003e2007\u003c/span\u003e). 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, \u003cspan class=\"CitationRef\"\u003e2020\u003c/span\u003e; Hamdi et al., \u003cspan class=\"CitationRef\"\u003e2021\u003c/span\u003e; Sakr et al., \u003cspan class=\"CitationRef\"\u003e1992\u003c/span\u003e; Wang and Croll, \u003cspan class=\"CitationRef\"\u003e2004\u003c/span\u003e). Developing larvae can reduce gonad volumes and alter hormonal homeostasis, leading to inhibition of egg production (Bayne and Loker, \u003cspan class=\"CitationRef\"\u003e1987\u003c/span\u003e). 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, \u003cspan class=\"CitationRef\"\u003e1995\u003c/span\u003e).\u003c/p\u003e\n\u003cp\u003e8.9. Impact of \u003cem\u003eSchistosoma\u003c/em\u003e infection on comet assay at 1st shedding stage.\u003c/p\u003e\n\u003cp\u003eThe 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., \u003cspan class=\"CitationRef\"\u003e2018\u003c/span\u003e), as well as DNA damage in Biomphalaria alexandrina homocytes (Mohamed, \u003cspan class=\"CitationRef\"\u003e2011\u003c/span\u003e) and hemocytes of infected Bulinus truncatus (Saad et al., \u003cspan class=\"CitationRef\"\u003e2013\u003c/span\u003e).\u003c/p\u003e\n\u003cp\u003e8.10. Impact of \u003cem\u003eS. mansoni\u003c/em\u003e with \u003cem\u003eB. alexandrina\u003c/em\u003e and \u003cem\u003eS. haematobium\u003c/em\u003e with \u003cem\u003eB. truncates\u003c/em\u003e on digestive and hermaphrodite gland at 1st shedding stage:\u003c/p\u003e\n\u003cp\u003eThe study found severe damage to the cell constituents of the digestive and hermaphrodite glands of infected \u003cem\u003eB. alexandrina\u003c/em\u003e and \u003cem\u003eB. truncatus\u003c/em\u003e 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., \u003cspan class=\"CitationRef\"\u003e2012\u003c/span\u003e). 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, \u003cspan class=\"CitationRef\"\u003e1977\u003c/span\u003e; Choubisa, \u003cspan class=\"CitationRef\"\u003e1988\u003c/span\u003e). Rediae engulf the host's digestive cells and utilize hydrolases for their extracellular digestion, contributing to physiological damages (Choubisa, \u003cspan class=\"CitationRef\"\u003e1988\u003c/span\u003e, 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, \u003cspan class=\"CitationRef\"\u003e1972\u003c/span\u003e).\u003c/p\u003e\n"},{"header":"Conclusion","content":"\u003cp\u003eThe present study suggests that changes in the behavior of \u003cem\u003eB. alexandrina\u0026nbsp;\u003c/em\u003eand \u003cem\u003eB. truncatus\u003c/em\u003e exposed to \u003cem\u003eS. mansoni\u003c/em\u003e and \u003cem\u003eS. haematobium\u003c/em\u003e, 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 \u003cem\u003eB. alexandrina\u003c/em\u003e and \u003cem\u003eB. truncatus\u003c/em\u003e .\u003c/p\u003e\n\u003cp\u003e\u0026nbsp;\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003eAcknowledgement\u003c/p\u003e\n\u003cp\u003eThis research did not receive any specific grant from funding agencies in the public, commercial, or\u003c/p\u003e\n\u003cp\u003enot- \u0026nbsp;for-profit sectors.\u003c/p\u003e\n\u003cp\u003eConflict of \u0026nbsp; interest. \u0026nbsp;The authors declare that they have no competing interests.\u003c/p\u003e\n\u003cp\u003eThis study was approved by Medical Malacology Department and received approval Scientific Ethics Committee by Theodor Bilharz \u0026nbsp;Research Institute (TBRI), Imbaba, Giza, Egypt .\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003eAbdel-Tawab, H, Ibrahim, AM, Hussein, T, Mohamed, F, (2022). Mechanism of action and toxicological evaluation of engineered layered double hydroxide nanomaterials in \u003cem\u003eBiomphalaria alexandrina\u003c/em\u003e snails. Environ. Sci. Pollut. Res. Int. 29. https://doi.org/10.1007/S11356-021-16332-W\u003c/li\u003e\n\u003cli\u003eAlberto-Silva AC, Santos EGN, Santos CP, Mello-Silva CC, (2015) Changes in the locomotory and reproductive behavior of Biomphalaria glabrata infected with Schistosoma mansoni. Exp. Parasitol 153, 68\u0026ndash;74. [PubMed: 25765559]\u003c/li\u003e\n\u003cli\u003eAlon G, Laureuce SS. and Sleinberge Y, (2007) Correlation between levels of sex hormones (progesterone, testosterone, and estrogen) and ecophysiological-behavior stages in two species of desert snails (Sphincterochila zonata and Sphincterochila prophetarum) in the Northern Negev Desert. General and Comparative Endocrinology 151(1):122-\u003c/li\u003e\n\u003cli\u003eAnderson RM, Mercer JG, Wilson RA, Carter NP, (1982) Transmission of Schistosoma mansoni from man to snail: experimental studies of miracidial survival and infectivity in relation to larval age, water temperature, host size and host age.\u0026nbsp;\u003cem\u003eParasitology.\u0026nbsp;\u003c/em\u003e;85:339\u0026ndash;360.\u0026nbsp;\u003c/li\u003e\n\u003cli\u003eArchibald RG, (1933) J. Trop. Med. Hyg., 36, 345.\u003c/li\u003e\n\u003cli\u003eBayne C, \u0026amp; Loker E, (1987) Survival within the Snail Host. The Biology of Schistosomes: from Genes to Latrines. pp. 321\u0026ndash;346.\u003c/li\u003e\n\u003cli\u003eBayne CJ, Yashino TP, (1989) Determination of compatibility in molluscatrematode parasitism. Amer Zoologist 29: 399-406.\u003c/li\u003e\n\u003cli\u003eBecker W, (1980) Metabolic interrelationship of parasitic trematodes and molluscs, especially Schistosoma mansoni in Biomphalaria glabrata. Z Parasitenkd 63 : 101 111.\u003c/li\u003e\n\u003cli\u003eBecker W, (1980) Microcolorimetric studies in Biomphalaria glabrata: The influence of Schistosoma mansoni on basal metabolism. Comp. Biochem. Physiol., 135(B): 101.\u003c/li\u003e\n\u003cli\u003eBeutler E, (1963) Improved method for determination of blood glutathione. J Lab Clin Med 61:882\u0026ndash;888.\u003c/li\u003e\n\u003cli\u003eBikowska EZ, (2006) Interakcje w ukl = adzie z_ywiciel \u0026ndash; pasoz_yt mie˛dzy bl =otniarkami Lymnaea stagnalis i przywrami z gatunko\u0026acute;w: Diplostomum pseudospathaceum, Echinoparyphium aconiatum, Plagiorchis elegans. Wydawnictwo Uniwersytetu Mikol=aja Kopernika, Torun.\u003c/li\u003e\n\u003cli\u003eChoubisa SL, \u0026amp; Sharma PN, (1986) Incidence of larval trematodes infection and their seasonal variation in the freshwater molluscs of southern Rajasthan. Rec Zool Surv India 83:69\u0026ndash;83.\u0026nbsp;\u003c/li\u003e\n\u003cli\u003eChoubisa SL (2008b) Mode of nutrition in pathogenic trematode larvae (redia and cercaria) which infect hepatopancreas of fresh water snails (Mollusca: Gastropoda). J Parasit Dis 32(1):68\u0026ndash;73\u003c/li\u003e\n\u003cli\u003eChoubisa SL,. ZulfiyaSheikh \u0026amp; Jaroli VJ, (2012) Histopathological effects of larval trematodes on the digestive gland of freshwater snail species, Vivipara bengalensis and Lymnaea acuminate . J Parasit Dis. 36(2):283\u0026ndash;286.\u003c/li\u003e\n\u003cli\u003eChoubisa SL. (1988) Histological and histochemical observations on the digestive gland of Melanoides tuberculatus (Gastropoda) infected with certain larval treamatodes and focus on their mode of nutrition. 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[PubMed: 15286820]\u003c/li\u003e\n\u003cli\u003eCroll RP, \u0026amp; Wang C, (2007) Possible roles of sex steroids in the control of reproduction in bivalve molluscs. Aquaculture 272, 76\u0026ndash;86.\u003c/li\u003e\n\u003cli\u003eCurtis LA, (1990) Parasitism and the movements of intertidal gastropod individuals. Biol Bull 179:105\u0026ndash;112.\u003c/li\u003e\n\u003cli\u003eCurtis LA, (1993) Parasite transmission in the intertidal zone: vertical migrations, infective stages, and snail trails. J Exp Mar Biol Ecol 173:197\u0026ndash;209.\u003c/li\u003e\n\u003cli\u003eDamerval C, De Vienne D, Zivy M, Thiellement H (1986) Technical improvements in two‐dimensional electrophoresis increase the level of genetic variation detected in wheat‐seedling proteins. Electrophoresis 7:52\u0026ndash;54. https://doi.org/10.1002/elps.1150070108\u003c/li\u003e\n\u003cli\u003eDe Jong-Brink M, (1995) How schistosomes profit from the stress responses they elicit in their hosts. Adv. Parasitol. Elsevier 177\u0026ndash;256.\u003c/li\u003e\n\u003cli\u003eDokmak HAAS, El-Emam MA, Mossalem HS, et al (2021). Impact of carbamide perhydrate on the snail Bulinus truncatus, the intermediate host of Schistosoma haematobium. Egyptian Journal of Aquatic Biology \u0026amp; Fisheries. Vol. 25(3): 85 \u0026ndash; 99\u003c/li\u003e\n\u003cli\u003eEl-Sayed K, El-Dafrawy S, Sharaf El-Din A, (1999). Influence of Schistosoma mansoni infection on Biomphalaria alexandrina snails under laboratory conditions. J. Zool. Egypt., 33: 343- 354\u003c/li\u003e\n\u003cli\u003eErasmus DA, (1972) The biology of trematodes. University Press, Belfast Frank GH (1963) Some factors affecting the fecundity of Biomphalaria pfeifferi (krauss). Bull World Health Organ 29:531\u0026ndash;537\u003c/li\u003e\n\u003cli\u003eFrank GH (1963) Some factors affecting the fecundity of Biomphalaria pfeifferi (krauss). Bull World Health Organ 29:531\u0026ndash;537\u003c/li\u003e\n\u003cli\u003eFryer SE, Oswald RC, Probert AJ, Runham NW, (1990) The effect of\u0026nbsp;\u003cem\u003eSchistosoma haematobium\u003c/em\u003e\u0026nbsp;infection on the growth and fecundity of three sympatric species of bulinid snails.\u0026nbsp;\u003cem\u003eJ. Parasitol\u003c/em\u003e\u0026nbsp;557\u0026ndash;563.\u0026nbsp;\u003c/li\u003e\n\u003cli\u003eGornowicz D, Dmochowska K, Bikowska EZ, and Towska KZOL, (2013) .Total antioxidative status and the activity of peroxidase and superoxide dismutase in the haemolymph of lymnaea stagnalis (l.) naturally infected with digenean trematodes Journal of Molluscan Studies. 79: 225\u0026ndash; 229.\u003c/li\u003e\n\u003cli\u003eGrazeffe, VS, De Freitas Tallarico L, De Sa Pinheiro A, et al (2008) .Establishment of the comet assay in the freshwater snail Biomphalaria glabrata (Say, 1818). Mutat Res Toxicol Environ Mutagen 654:58\u0026ndash;63.\u003c/li\u003e\n\u003cli\u003eHabib MR, Ghonamea SI, Alia RE,. Gad El-Karima RM, Youssefa, AA, Crollb RP, Millerc, MW. (2020) Biochemical and apoptotic changes in the nervous and ovotestis tissues of Biomphalaria alexandrina following infection with Schistosoma mansoni0). Exp Parasitol. 213: 107887. doi:10.1016/j.exppara.2020.107887.\u003c/li\u003e\n\u003cli\u003eHadas E, \u0026amp; Stankiewicz M, (1996) Strategies of biochemical defence mechanisms of parasites against oxidants and free radicals Acta Parasitologica, 41: 1\u0026ndash;6.\u003c/li\u003e\n\u003cli\u003eHamdi SAH, Ibrahim AM, Ghareeb MA, Fol MF (2021) Chemical characterization, biocidal and molluscicidal activities of chitosan extracted from the crawfish Procambarus clarkii (Crustacea: Cambaridae). 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Geneva, Switzerland: WHO, 2013. 2.\u003c/li\u003e\n\u003c/ol\u003e"},{"header":"Plates","content":"\u003cp\u003ePlates 1 and 2 are available in the Supplementary Files section\u003c/p\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"acta-parasitologica","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"actp","sideBox":"Learn more about [Acta Parasitologica](http://link.springer.com/journal/11686)","snPcode":"11686","submissionUrl":"https://submission.springernature.com/new-submission/11686/3","title":"Acta Parasitologica","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"stoa","reportingPortfolio":"Springer Hybrid","inReviewEnabled":true,"inReviewRevisionsEnabled":false},"keywords":"Biomphalaria alexandrina, Bulinus truncatus, genotoxic effect, food behavior, Schistosoma haematobium, Schistosoma mansoni","lastPublishedDoi":"10.21203/rs.3.rs-3110632/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-3110632/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eTrematodes infection of genus \u003cem\u003eSchistosoma\u003c/em\u003e 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 \u003cem\u003eBiomphalaria alexandrina\u003c/em\u003e and \u003cem\u003eBulinus truncatus\u003c/em\u003e during the shedding stage of infection with \u003cem\u003eSchistosoma mansoni\u003c/em\u003e and \u003cem\u003ehaematobium\u003c/em\u003e, respectively. The study found that the infection rate with \u003cem\u003eS. mansoni\u003c/em\u003e was 34.7% and 30.4% with \u003cem\u003eS. haematobium\u003c/em\u003e. In \u003cem\u003eB.alexandrina\u003c/em\u003e infected with \u003cem\u003eS. mansoni\u003c/em\u003e, a survival rate of 65.2% was recorded, along with a mean duration of shedding of 32.8\u0026thinsp;\u0026plusmn;\u0026thinsp;5.5 days, a mean prepatent period of 37.5\u0026thinsp;\u0026plusmn;\u0026thinsp;1.15 days, and a mean life span of 57.0\u0026thinsp;\u0026plusmn;\u0026thinsp;1.21 days. Meanwhile, in \u003cem\u003eB. truncatus\u003c/em\u003e infected with \u003cem\u003eS. haematobium\u003c/em\u003e, a survival rate of 56.4% was recorded, with a mean duration of shedding of 42.6\u0026thinsp;\u0026plusmn;\u0026thinsp;2.6 days, a mean prepatent period of 46.7\u0026thinsp;\u0026plusmn;\u0026thinsp;2.3 days, and a mean life span of 65.9\u0026thinsp;\u0026plusmn;\u0026thinsp;1.6 days.\u003c/p\u003e \u003cp\u003eThe feeding behavior was increased in the two infected species snail, while the net reproductive rate (R\u003csub\u003eo\u003c/sub\u003e) 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 \u003cem\u003eB. alexandrina\u003c/em\u003e and increased in infected \u003cem\u003eBulinus\u003c/em\u003e. Steroid hormone measurements were increased in the infected \u003cem\u003eBiomphalaria\u003c/em\u003e, while they were reduced in infected \u003cem\u003eBulinus\u003c/em\u003e. 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 \u003cem\u003eB. alexandrina\u003c/em\u003e and \u003cem\u003eB. truncatus.\u003c/em\u003e\u003c/p\u003e","manuscriptTitle":"Impact of Schistosoma sp., infection on biological, behavioral, physiological, histological, and genotoxicological aspects of Biomphalaria alexandrina and Bulinus truncatus snails","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2023-07-25 13:30:33","doi":"10.21203/rs.3.rs-3110632/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"reviewerAgreed","content":"","date":"2023-08-30T14:21:01+00:00","index":0,"fulltext":""},{"type":"reviewersInvited","content":"","date":"2023-07-19T09:11:47+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2023-07-03T02:55:48+00:00","index":"","fulltext":""},{"type":"submitted","content":"Acta Parasitologica","date":"2023-06-27T19:09:39+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"acta-parasitologica","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"actp","sideBox":"Learn more about [Acta Parasitologica](http://link.springer.com/journal/11686)","snPcode":"11686","submissionUrl":"https://submission.springernature.com/new-submission/11686/3","title":"Acta Parasitologica","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"stoa","reportingPortfolio":"Springer Hybrid","inReviewEnabled":true,"inReviewRevisionsEnabled":false}}],"origin":"","ownerIdentity":"2bb7a794-269c-496d-b743-03e03d5d90b4","owner":[],"postedDate":"July 25th, 2023","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[],"tags":[],"updatedAt":"2024-02-05T15:07:17+00:00","versionOfRecord":{"articleIdentity":"rs-3110632","link":"https://doi.org/10.1007/s11686-023-00760-4","journal":{"identity":"acta-parasitologica","isVorOnly":false,"title":"Acta Parasitologica"},"publishedOn":"2024-02-01 15:01:36","publishedOnDateReadable":"February 1st, 2024"},"versionCreatedAt":"2023-07-25 13:30:33","video":"","vorDoi":"10.1007/s11686-023-00760-4","vorDoiUrl":"https://doi.org/10.1007/s11686-023-00760-4","workflowStages":[]},"version":"v1","identity":"rs-3110632","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-3110632","identity":"rs-3110632","version":["v1"]},"buildId":"7rjqhiLT3MXkJMwkYKINL","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}