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Snails and fish as pollution biomarkers in Lake Manzala and laboratory a: Lake Manzala snails.

Introduction

Lake Manzala is considered one of the most important lakes in Egypt. It is exposed to high levels of pollutants from industrial, domestic and agricultural resources [1-3]. Ali reported that Lake Manzala receives about 4000 million cubic meters of untreated industrial, domestic and agricultural waste water annually [4].

The use of physiological and biochemical parameters as indicators of water quality has been developed to detect sublethal impacts of pollutants. Prominent among these biomarkers are physiological variables, such as plasma levels of metabolites [5], haematological data [6,7], levels of hormones [8-11] and biochemical variables such as detoxifying enzyme activities [12,13]. Interesting reports concerning the mechanisms of metal uptake, accumulation, transport, and elimination of metals in molluscs are usually focused on chemical, biochemical, molecular, and physiological aspects [14-21]. El-Khayat assessed genetic variation and genetic pattern of Lymnaea snails collected from irrigation canals in four different Governorates using ISSR markers, with the characterization of environmental parameters of the collecting Lymnaea sites. The authors showed high polymorphism by using for the first time the ISSR PCR technique for studying genetic variations of L. natalensis snails in Egypt and concluded that L. natalensis snails can survive associated with other snails, plants, and insects and can be tolerate the heavy metals in water [22].

Similarly, histopathological changes have been widely used as biomarkers in the health evaluation of animal organisms. The discharge of toxic elements into the rivers, estuaries and coastal waters poses serious pollution and consequently affects the fish, flora and fauna as snail.

Moreover, freshwater molluscs play an important role in aquatic ecosystems, providing food for many fish species and vertebrates [23].

This work aims to record the alterations of the Physiological, hematological and histopathological parameters in snails collected from Lake Manzala as a bio-indicator for water pollution.

Materials and Methods

Snail samples were collected from 8 sites in Lake Manzalafrom 3 governorates; Port-Said (Kobry El-Lansh, Kaar El-Bahr and El-Khankak), Dakahlya (Gammalya, Matarya and Nasayma) and Damietta (Ananyya and Sayala). The snails collected were kept in water from their habitat and examined for natural infection. The negative (uninfected) Biomphalaria snails and other collected species (Physa and Planorbis) were contributed in the physiological studies. On the other hand, both negative and positive Biomphalaria samples were examined histologically.

Biochemical studies

Determination of liver and kidney functions: The assessment of aspartate aminotransferase (AST), alanine aminotransferase (ALT), alkaline phosphatase (ALP), urea, creatinine, total and direct bilirubin, albumin (ALB) and total protein were examined in snail tissue extracts. They were assayed biochemically using biosystem autoanalyzer, Backmann at Theodor Bilhaz Institute (TBRI) hospital laboratories. Snail tissues were dissected out, homogenized in bi-distilled water (1:1 w/v) using motor homogenizer and centrifuged at 5000 rpm for 20 min at 4[degrees]C and the supernatants were taken and kept at -20[degrees]C till used as described by [24].

Creatinine was determined according to [25]. In this method, creatinine reacts with picrate to form a coloured complex and the rate of formation of the complex is measured photometrically at 492 nm.

Urea was determined by using the coupled urease/glutamate dehydrogenase (GLDH) enzyme system according to [26].

Determination of antioxidant enzymes: The antioxidant enzymes catalase (CAT), Glutathione-S-Transferase (GST) and Gamma Glutamyltransferase (GGT) were assayed in snail tissue extract using spectrophotometer. Snail's tissues were dissected out. Each snail tissue from each treatment was homogenized in bi-distilled water (10:1 w/v) using motor homogenizer. Homogenates were centrifuged at 5000 rpm for 20 min at 4[degrees]C and the supernatants were taken and kept at -20[degrees]C till used.

Determination of snail hemolymph components: Snail hemolymph was collected in accordance to the technique of [27]. The hemolymph was obtained via small hole made in the shell into which capillary tube was inserted then it was drawn into tube by capillary suction. The hemocytes of the samples hemolymph were determined by haemocytometer. For total and differential counting, monolayer of hemocytes were stained with Giemsa stain for 20 minutes, according to the methods of [28] and counted by light microscopy.

Histopathological examinations: Snail specimens collected from Lake Manzala were dissected, removed from their shells gently and fixed in 10% buffered neutral formalin solution. Five-micron thick paraffin sections were prepared, stained by hematoxylin and eosin (HE) and then examined microscopically and photographed for histopathology observations [29].

Statistical analysis: Data are expressed as means [+ or -] SD. The results were computed statistically (SPSS software package, version 20) using the T-test analysis. Values of p<0.05 were considered statistically significant.

Results

Biochemical parameters

The present results showed significant increase in AST, ALT, and

ALP in Planorbis and Physa, respectively in most samples collected from Nasayma site in Lake Manzala. Most of snails collected from Port-Said and Dakahlya sites showed significant increase in urea. Results of creatinine in samples from different lake sites showed alteration, ranged between non-significant decrease and increase (Table 1). Significant increase of total protein level was obtained in all field samples while total bilirubin showed the highest levels in physa and planorbis samples collected from Nasayma, Dakahlya and in Biomphalaria samples collected from Matarya, Dakahlya. Also, results showed higher levels of indirect bilirubin than direct. Most snail samples showed approximately normal A/G ratio (Table 2).

Antioxidant enzymes

Significant alterations in catalase (CAT) level were noticed in all snail samples collected from Lake Manzala as compared with lab bread controls (except in Planorbis collected from Kobry El-Lansh and Biomphalaria from Gammalya and Biomphalaria from Nasayma). The recorded alterations in the snail samples was increased by 18 to 185%, or decreased by -13 to -90% (Table 3).

Glutathione-S-transferase (GST) alteration was demonstrated in all samples includes decrease in activity ranging from -21% to -83% (P<0.001) and increase in activity ranging from 13% to 119%.

The same result was noticed in Gamma-glutamyl transpeptidase (GGT) in snail samples as compared with lab bread controls, some samples showed decrease change activity ranging from -1% to -35% and other samples showed increase change activity ranging from 6% to 666%, (Table 3).

Determination of hemolymph components

The majority of snail samples showed significant decrease in total and differential cell count as compared with lab bread controls (Table 4). The higher percent of decrease in the total cell count (-72%) was recorded in Biomphalaria collected from Nasayma, Dakahlya. Hemoglobin concentration showed alteration; increased to 2.6 g in Planorbis collected from Kobry El-Lansh and decreased to 0.8 g in Physa collected from Annanya, Damietta.

The histopathological observations

A knowledge of the normal histology and structure of snails is guided by [30].

Head foot: The normal foot region has an outer cuticular layer as a protective layer of the foot. Inner to this lining there is a tall columnar epithelium with basal nuclei in its cell. Amongst the columnar epithelium there are modified sacs like cells in the form of unicellular glands which open through the cuticular layer exterior to the foot surface. These unicellular glands are involved in mucous secretion. Embedded in between there are transversely muscle fibers, called as longitudinal muscle fibers. Major part of the foot muscles are made up of thickly arranged oblique muscle fibers.

Histopathological observations in foot region of Biomphalaria snail samples showed necrotic change (shrinkage) in the mucous secreting unicellular glands (Figure 1b) and hyaline substances are shown in samples collected from Port Said (Figure 1c) and splitting fiber tissues in Dakahlya and Damietta snails (Figure 1d,1e). Also, results showed oblique splitting muscle fibers, increased empty spaces and atrophy within muscles of snail head in Dakahlya samples (Figure 1f,1g,1h).

Salivary gland: The normal salivary gland of B. alexandrina snail composed of two lobs found in the buccal mass as shown in (Figure 2a).

The histopathological effects of polluted water showed shrinkage and atrophy in the salivary gland of snails collected from Damietta (Figure 2b), focal areas of necrosis (Figure 2c,2d), large fat vacuoles (Figure 2e) and enlargement of the salivary gland (Figure 2f) in snails collected from Port said.

Central ganglia: The central nervous system ganglia are in the form of compact mass of ring surrounding the esophagus of the snail. (Figure 3) showed that all ganglia exhibit presence of enlarged neurosecretory neurons (Figure 3a). Fibrosis (Figure 3b,3c) and degeneration with large vacuoles (Figure 3d) were observed in snail samples collected from Damietta and Dakahlya (Figure 3).

Hepatopancreas: The normal histological structure of Biomphalaria hepatopancreas includes glandular tubules interspersed with connective tissues. The entire gland is enclosed within a thin walled sac called as tunica propria. The hepatopancreatic epithelium is rested on thin basement membrane; at least 3-4 types of cells can be recognized in the hepatopancreatic epithelium of the snail, digestive, calcium and excretory cells (Figure 4a). The histopathological changes showed cellular necrosis followed by loss of secretory activity of the epithelial cells in Port Said samples (Figure 3b). Also, atrophy, degeneration and fat vaculation were noticed in Port Said and Damietta samples (Figure 4c,4d). Dilated lumen and more than two hepatopancreatic tubules connected together with one larger lumen in Dakahlya samples (Figure 4e,4f).

Male organs (Prostate gland): The normal histological structures of the male organs of B alexandrina composed mainly of sperm duct and the prostate tubules (Figure 5a).

The histopathological observations of Port Said samples showed severe dilated sperm duct and prostate tubules, dilated lumen of prostate tubules which filled with hyaline and degeneration wall with necrotic change (Figure 5b,5c). while Dakahlya samples showed enlarged sperm duct, degenerated prostate tubules and clogged sperms.

[FIGURE 1 OMITTED]

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[FIGURE 3 OMITTED]

The prostate gland in Damietta samples showed severe degeneration and atrophy (Figure 5b,5c).

The hermaphrodite gland: Histology of normal hermaphrodite gland of the adult B. alexandrina snails as that of any other pulmonate snail consists of number of vesicles known as acini separated from each other by thin vascular connective tissue (Figure 6a). Each acinus is enveloped in a sheath of squamous epithelium. In each acinus both male and female reproductive gametes are produced where mature ova are located at the periphery of the acini and bundles of male sperms are arranged in the center. Various stages of sperm and ovum development (simultaneous) are evident.

Histopathological alteration in Port Said samples included, acini lost their normal architechture and their separating connective tissues are almost degenerated (Figure 5b). The acinar epithilum showed necrotic changes in the form of decreasing cytoplasm of oocytes and partial destruction (Figure 6c). Atrophy and reduction in the number of sperms was also observed (Figure 6d). Degenerative changes were observed in most of the ova, where some of them have faint staining nuclei and others lost their nucleous (Figure 6e,6f). Some acini appear more or less evacuated and large fat vacuoles can be seen in Dakahlya samples (Figure 6g). Damietta showed the most degenerated features in the hermaphrodite gland as atretic oocytes and sperms and atrophy of most gland components (Figure 6h,6i).

[FIGURE 4 OMITTED]

[FIGURE 5 OMITTED]

[FIGURE 6 OMITTED]

The infected Biomphalaria samples collected from lake manzala

Some of Biomphalaria samples collected from Dakahlya and Port Said showed the presence of parasite sporocycts.

The oblique muscle fiber got damaged and mother sporocysts take place within foot muscles, thereby causing splitting, necrosis and increased empty spaces within muscle fibers (Figure 7a-7c).

The digestive gland was destructed while daughter sporocycts which contain many developing cercariae were noticed. The histopathological changes of digestive gland of B. alexandrina induced exudation in the lumen of tubules, expansion of hemolymphatic spaces between the tubules, loosing of connective tissue and increase of vaculation and necrotic changes in the digestive cells (Figure 7d,7e,7f).

Accumulation of heavy metals in snail tissues

(Figure 8) showed the accumulation of heavy metals in head foot tissues of Biomphalaria snails collected from Port Said, Damietta and Dakahlya samples.

Discussion

Under conditions of pollution mollusks are susceptible to the pathogenic effects of toxicants, which in turn may result in detrimental changes to their immunological and physiological processes [31].

The present results showed significant increase in AST and ALT, and ALP in Planorbis and Physa snail samples, collected from Nasayma site in Lake Manzala. Moreover, the results showed alterations in CAT, GST and GGT activity in snail samples collected from Lake Manzala.

AST and ALT are vital enzymes in the metabolism and generation of energy from amino acids [32]. Therefore, the elevated transaminases may indicate the high energy demand of the snail under stressful conditions of intoxication. Also, the increase in ALT, AST and ALP enzymes were correlated with alteration in phospholipid metabolism [33] which indicated mainly to hepatocellular disorder [34]. Under physiological stress conditions in animals, the catalytic activity of the urea pathway enzymes is also accelerated [35].

These results are in agreement with [36] who recorded a significant increase of transaminases activity and catalase in the garden snail specimens (Helix pomatia L) which were collected from polluted area compared to control. Also, [37] indicated that there are significant elevations in the levels of acid phosphatase and alkaline phosphatase, after using of Profenophos against B. alexandrina, which can be explained by the destruction of internal snail cells. Mohamed revealed an elevation in the activities of AST, AlT and AkP enzymes in snails' tissues post treatment with [LC.sub.10] and [LC.sub.25] of Basudin, Selecron and Bayluscide in comparison with control groups [38]. Some other authors recorded increase of the activity of these enzymes, while others recorded decrease in intoxicated animals [36,39,40]. Abdel-Daim reported increased serum AST, ALT, ALP, cholesterol, urea, uric acid, creatinine and tissue MDA after application of deltamethrin subacute intoxication (1.46 [micro]g/L for 28 days) against Oreochromis niloticus fish [41]. At the same time they found that tissue levels of GSH, GSH-Px, SOD and CAT were reduced. On the other hand, [42] recorded suppression of the antioxidant enzyme activity and alterations of serum biochemical parameters in freshwater fish Nile tilapia, Oreochromis niloticus.

[FIGURE 7 OMITTED]

[FIGURE 8 OMITTED]

Significant increase of total protein level was recorded also in all samples collected from Lake Manzala. This increase may be attributed to the changes in hepatic protein synthesis [43,44] due to the stress in the polluted habitat. These results go in the same direction as those of [45] who recorded an increase in the total protein concentration in Helix snails dependent in the presence of metal dust. Also, [46] highlighted a significant increase in the total protein rate under the effect of a chemical stress at different biological models. Mello observed significant changes in protein metabolism in response to exposure to different concentrations of E. splendens var. hislopii latex, with significant increases in snails exposed to 0.8 and 1.0 mg/l of the latex, indicating latex toxicity [47]. The same was observed by [48] using other plants and higher concentrations.

Snails collected from most Port-Said and Dakahlya sites showed significant increase in urea. Urea is only synthesized in liver from excess amino acids and excreted by kidney and major illness may increase urea levels [49]. The variation in the nitrogen degradation products showed that the increase of urea content occurred when the uric acid level declined. In accordance with this, the exposure of Biomphalaria glabrata to Euphorbia splendens var. hislopii latex caused the urea content increased which reflects a disturbance in the snail's regulation of their metabolism due to intoxication caused by the latex exposure [50].

Snail samples collected from most sites of Lake Manzala showed significant decrease in total hemolymph cell count, hyalinocytes, round small hemocytes and granuolocytes. The decrease in hemolymph cells may be considered as a haemolysis response to the multiple pollution elements in Lake Manzala. This was mentioned by [51] that haemocytosis represents a response to external stress or certain stimuli and may originate from a variety of biotic or abiotic sources [52]. These results were in agreement with [53] who found that exposure to dyestuff and chemical effluent could result in decreases in RBC count and Hb content which are symptoms of anemia.

The histopathological changes produced by pollutants in organs and tissues can occur before they produce irreversible effects on the biota. So, histological methods can be used in conjunction with other parameters and/or ecotoxicological bioindicators as an early warning system for the survival of the species, as well as for environmental protection.

Histopathological observations in head foot region of Biomphalaria snails showed shrinkage in the mucous secreting unicellular glands and hyaline substances in samples collected from Port Said sites, splitting fiber tissues, increased empty spaces and atrophy within muscles of snail head in Dakahlya and Damietta samples. The salivary gland of snails collected from Damietta showed shrinkage and atrophy while there were focal areas of necrosis, large fat vacuoles and enlargement of the salivary gland in snails collected from Port Said. All snails ganglia showed modified and enlargement of neurons, degeneration with large vacuoles and fibrosis in samples collected from Damietta and Dakahlya. The histopathological changes of hepatopancreas included cellular necrosis followed by loss of the epithelial cells were shown in Port Said samples. Also, atrophy, degeneration and fat vaculation were noticed in Port Said and Damietta samples. Dilated lumen and more than two hepatopancreatic tubules connected together with one larger lumen in Dakahlya samples. The prostate gland in snails of Port Said samples showed severe dilated sperm duct and prostate tubules, dilated lumen of prostate tubules which filled with hyaline and degeneration wall with necrotic change. While Dakahlya samples showed enlarged sperm duct, degenerated prostate tubules and clogged sperms. The prostate gland in Damietta samples showed severe degeneration and atrophy. Regarding the hermaphrodite gland in Dakahlya samples, decreasing cytoplasm of oocytes, partial destruction, lost nucleus, large fat vacuoles, atrophy and reduction in the number of sperms were observed. Damietta samples showed the most degeneration features in the hermaphrodite gland as atretic oocytes and sperms and atrophy of most gland components.

All these histopathological damages in snail organs may be due to the pollution of Lake Manzala water by heavy metals which recorded by [22]. Stress responses in invertebrates can occur following acute or chronic exposures to contaminated environments and as such, the overall health status of individuals within those environments, both in terms of histopathological lesions and the presence of infecting organisms, may ultimately reflect the general health status of these sites [54].

The digestive glands of molluscs have been known as target organs for contaminant effects because; this organ plays a major role in contaminant uptake, intracellular food digestion and metabolism of inorganic and organic chemicals in the organisms [55-57]. However, particulate metal uptake is mainly achieved via the digestive tract by endocytosis; further metals are transferred first to lysosomes and then to residual bodies, especially in the digestive cells of the digestive gland [58]. It could also be possible that in the damage in the snail's hepatopancreas including the alteration of liver and kidney enzymes is according to functionality analog with vertebrate's liver that accumulate mostly heavy metals compared to other organs, and which damage it also [59,60].

In agreement of these results, the exposure of the snails Archachatina marginata to sublethal concentrations of the metals resulted in a prevalence of hepatocellular foci of cellular alterations (FCA) in the hepatopancreas of snails. Basophilic adenoma and ovotesticular fibrillar inclusions were also observed in the ovotestes of snails exposed to the test metals [61]. Jonnalagadda have been reported histopathological alterations such as degeneration and the gathering of amebocytes in areas between the tubules in the digestive gland of snail Bellamya dissimilis exposed to endosulfan [62]. The histopathological examinations of Lymnaea luteola exposed to Paraquat (Gramoxone) revealed the following changes: amebocytes infiltrations, the lumen of digestive gland tubule was shrunken; degeneration of cells, secretory cells became irregular, necrosis of cells and atrophy in the connective tissue of digestive gland [63]. Moreover, it is worthy to mention that in the freshwater snails nervous system has been proved to be sensitive to many toxic materials and cytotoxicants that may induce injurious consequences [64-66].

Some of Biomphalaria samples collected from Dakahlya and Port Said showed the presence of parasite sporocycts. The most histopathological deleterious effects have been noticed within the tissues caused in the foot and hepatopancreas due to the invasion of larval trematode parasites to the host snail B. alexandrina. The oblique muscle fiber got damaged may be due to penetration of miracidia at the time of infection in the nature. Since earlier stages of larval development i.e. sporocyst and mother sporocyst, takes place within foot muscles, thereby causing increased empty spaces within muscle fibers after their entry in to the viscera of the snail. The digestive tubules epithelium got damaged to the extent of loss of normal tubular structure may be due to metabolic and other excretory materials in the form of granules found scattered in the connective tissue. The destruction of the digestive gland was even more severe may be due to the developing of daughter sporocycts which contains many of the developing cercariae.

Similar observations were recorded by [61] in the snail Archachatina marginata that the digestive gland tubule becomes compressed thereby resulting reduced tubular lumen of the gland as observed by that more cercaria and rediae were found in between the hepatic tubules and tunica propria causing extension of the space between tubules.

The histological observations of Biomphalaria snails collected from Lake Mazala showed accumulation of heavy metals in the head foot tissues. This was proved in the study of [22] who recorded that the metals concentrations were higher in snail tissues and water samples from Lake Manzala. The collected water samples from Damietta sites showed the highest significant Cu & Cd concentration while Port-Said samples showed the highest Pb concentration and Dakahlia showed the highest Zn concentration.

In conclusion, the severe alterations and degeneration recorded in the physiological and hematological parameters and also histopathological observations are clear evidence for the pollution of the water from which these snail samples were collected. This conclusion is confirmed by [67] who recorded highly significant concentrations of Cu, Cd, Pb and Zn in water samples from different Lake Manzala sites. Also, these metals were highly concentrated in snail and fish tissues and the higher metal bioaccumulation was determined in snails collected from sites showed higher water metals concentrations.

Abbrevations: AST: Aspartate Aminotransferase; ALT: Alanine Aminotransferase; ALP: Alkaline Phosphatase; ALB: Albumin; CAT: Catalase; GST: Glutathione-S-Transferase; GGT: Gamma Glutamyltransferase; TBRI: Theodor Bilhaz Institute; HE: Hematoxylin and Eosin Stain; A/G ratio: Albumin/Glubuline ratio

http://dx.doi.org/ 10.4172/2150-3508.1000153

Acknowledgement

This study is a joint project (Biomarkers as indicators of environmental pollution: Experimental approach and case studies), kindly funded by the Academy of Scientific Research and Technology through the Bilateral Agreement between Academy of Scientific Research and Technology of the Arab Republic of Egypt and Bulgarian Academy of Sciences (2012-2014).

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[67.] El-Khayat HMM, Mahmoud KMA, Gaber HS, Abdel-Hamid H, Abu Taleb HMA (2015b) Studies on the effect of pollution on Lake Manzala ecosystem in portsaid, damietta and Dakahlya governorates, Egypt. J. Egypt. Soc. Parasitol. (JESP). 45: 155-168.

Hanaa MM El-Khayat (1), Hoda Abdel-Hamid (1), Hanan S Gaber (2), Kadria MA Mahmoud (1) and Hassan E Flefel (1)

(1) Department of Environmental Researches and Medical Malacology, Theodor Bilharz Research Institute, Imbaba, PO Box-30, Giza, Egypt

(2) National Institute of Oceanography and Fisheries, Cairo, Egypt

* Corresponding author: Hanaa MM El-Khayat, Department of Environmental Researches and Medical Malacology, Theodor Bilharz Research Institute, Imbaba, PO Box-30, Giza, Egypt, Tel: 202 354 01019; E-mail: hanaamahmoud@hotmail.com

Received September 29, 2015; Accepted December 11, 2015; Published December 16, 2015
Table 1: Aspartate amino transferase (AST), alanine amino
transferase (ALT) alkaline phosphatase (ALP), glucose,
creatinine and urea in tissue extract of snails collected
from Lake Manzala.

Parameter                                       AST (Unites/ml)

Treatments                                Mean [+ or -]      Change
                                                SD             %

Control lab                              21.9 [+ or -] 4

Bort-Said   Kaar         Biomphalaria    26.2 [+ or -] 2       20
              El-Bahr    Planorbis       30.2 [+ or -] 4       38
            El-Khankak   Biomphalaria    11 [+ or -] 0 **     -50
            Kobry        Biomphalaria   37.4 [+ or -] 5 *      71
              El-Lansh   Planorbis      40.5 [+ or -] 6 *      85
Dakahlya    Gammalya     Biomphalaria   31.1 [+ or -] 0 **     42
            Nasayma      Biomphalaria   29.6 [+ or -] 3 *      35
                         Planorbis      56.4 [+ or -] 2 **    158
                         Physa          53.8 [+ or -] 3 **    146
            Matarya      Biomphalaria   32.1 [+ or -] 2 *      47
Damietta    Annanya      Physa           34.2 [+ or -] 5       56
            Sayala       Planorbis       30.6 [+ or -] 4       40

Parameter                                      ALT (Unites/ml)

Treatments                                Mean [+ or -]     Change
                                               SD             %

Control lab                             41.5 [+ or -] 10

Bort-Said   Kaar         Biomphalaria   64.3 [+ or -] 24      55
              El-Bahr    Planorbis       50.6 [+ or -] 7      22
            El-Khankak   Biomphalaria    57.9 [+ or -] 0      40
            Kobry        Biomphalaria   74.8 [+ or -] 12      80
              El-Lansh   Planorbis      65.7 [+ or -] 11      58
Dakahlya    Gammalya     Biomphalaria    65 [+ or -] 15       57
            Nasayma      Biomphalaria   44.1 [+ or -] 10      6
                         Planorbis      85.8 [+ or -] 9 *    107
                         Physa          66.4 [+ or -] 10      60
            Matarya      Biomphalaria    44 [+ or -] 17       6
Damietta    Annanya      Physa           53.6 [+ or -] 7      29
            Sayala       Planorbis       51.2 [+ or -] 8      23

Parameter                                           ALP (IU/L)

Treatments                                  Mean [+ or -]       Change
                                                 SD               %

Control lab                                38.4 [+ or -] 8

Bort-Said   Kaar         Biomphalaria      42.5 [+ or -] 4        11
              El-Bahr    Planorbis        56.8 [+ or -] 11        48
            El-Khankak   Biomphalaria     106 [+ or -] 0.0       176
            Kobry        Biomphalaria     94.0 [+ or -] 29       145
              El-Lansh   Planorbis       101.4 [+ or -] 11 *     164
Dakahlya    Gammalya     Biomphalaria     65.5 [+ or -] 10        71
            Nasayma      Biomphalaria      52.0 [+ or -] 4        35
                         Planorbis       105.6 [+ or -] 10 *     175
                         Physa          162.3 [+ or -] 4.7 **    323
            Matarya      Biomphalaria    66.3 [+ or -] 3.3 *      73
Damietta    Annanya      Physa           112.7 [+ or -] 4 **     193
            Sayala       Planorbis        57.9 [+ or -] 11        51

Parameter                                            Glucose

Treatments                                 Mean [+ or -]      Change
                                                SD              %

Control lab                               45.0 [+ or -] 8

Bort-Said   Kaar         Biomphalaria    76.1 [+ or -] 27       69
              El-Bahr    Planorbis       72.4 [+ or -] 11       61
            El-Khankak   Biomphalaria    85.7 [+ or -] 0.0      90
            Kobry        Biomphalaria    99.2 [+ or -] 6 *     120
              El-Lansh   Planorbis      96.8 [+ or -] 13 *     115
Dakahlya    Gammalya     Biomphalaria    91.0 [+ or -] 23      102
            Nasayma      Biomphalaria    80.1 [+ or -] 19       78
                         Planorbis      131.1 [+ or -] 6 **    191
                         Physa          119.3 [+ or -] 9 *     165
            Matarya      Biomphalaria   85.3 [+ or -] 3.1 *     90
Damietta    Annanya      Physa           66.4 [+ or -] 12       48
            Sayala       Planorbis       67.4 [+ or -] 16       50

Parameter                                      Creatinine (mg/dl)

Treatments                                Mean [+ or -]      Change
                                                SD             %

Control lab                             0.55 [+ or -] 0.22

Bort-Said   Kaar         Biomphalaria   0.35 [+ or -] 0.0     -36
              El-Bahr    Planorbis        0 [+ or -] 0.0      -100
            El-Khankak   Biomphalaria   1.46 [+ or -] 0.0     165
            Kobry        Biomphalaria     0 [+ or -] 0.0      -100
              El-Lansh   Planorbis      1.53 [+ or -] 1.25    178
Dakahlya    Gammalya     Biomphalaria   0.40 [+ or -] 0.04    -27
            Nasayma      Biomphalaria   1.31 [+ or -] 0.94    138
                         Planorbis      0.38 [+ or -] 0.0     -31
                         Physa          1.41 [+ or -] 0.0     156
            Matarya      Biomphalaria   0.12 [+ or -] 0.0     -78
Damietta    Annanya      Physa          0.08 [+ or -] 0.0     -85
            Sayala       Planorbis        0 [+ or -] 0.0      -100

Parameter                                           urea (mg/dl)

Treatments                                 Mean [+ or -]       Change
                                                 SD              %

Control lab                                9.4 [+ or -] 1

Bort-Said   Kaar         Biomphalaria     13.8 [+ or -] 1        47
              El-Bahr    Planorbis        12.4 [+ or -] 0        32
            El-Khankak   Biomphalaria    30 [+ or -] 0.0 *      219
            Kobry        Biomphalaria   27.3 [+ or -] 1.2 **    190
              El-Lansh   Planorbis      25.9 [+ or -] 1.1 **    176
Dakahlya    Gammalya     Biomphalaria   22.9 [+ or -] 13 **     144
            Nasayma      Biomphalaria     15.7 [+ or -] 3        67
                         Planorbis       19.3 [+ or -] 2 *      105
                         Physa           20.4 [+ or -] 2 *      117
            Matarya      Biomphalaria     22.8 [+ or -] 8       143
Damietta    Annanya      Physa            14.5 [+ or -] 3        54
            Sayala       Planorbis        12.3 [+ or -] 1        31

*, ** & *** significant compared to control value at p<0.05, p<0.01 &
p<0.001, respectively.

Table 2: Total protein, Albumin, globulin, A/G ratio, total
Bilirubin, direct and indirect in tissue extract of snails collected
from Lake Manzala.

Parameter                            Total protein (g/dl)

Treatments                              Mean [+ or -] SD      Change
                                                                %
Control lab                            6.21 [+ or -] 0.1

Bort-      Kaar       Biomphalaria   10.35 [+ or -] 0.4 **      67
  Said     El-Bahr    Planorbis      11.97 [+ or -] 0.6 **      93

           El-        Biomphalaria   12.42 [+ or -] 0.04 **    100
           Khankak

           Kobry      Biomphalaria   12.39 [+ or -] 0.8 **     100
           El-        Planorbis      10.86 [+ or -] 0.6 **      75
           Lansh
Dakahlya   Gammalya   Biomphalaria   11.49 [+ or -] 0.3 **      85
           Nasayma    Biomphalaria   23.04 [+ or -] 0.5 ***    271
                      Planorbis      24.27 [+ or -] 0.7 ***    291
                      Physa           8.94 [+ or -] 0.2 **      44
           Matarya    Biomphalaria   11.67 [+ or -] 0.59 **     88
Damietta   Annanya    Physa            9.9 [+ or -] 0.6 *       59
           Sayala     Planorbis

Parameter                                          Albumin (g/dl)

Treatments                              Mean [+ or -] SD       Change
                                                                 %
Control lab                            3.27 [+ or -] 0.02

Bort-      Kaar       Biomphalaria    6.84 [+ or -] 0.30 **     109
  Said     El-Bahr    Planorbis       5.52 [+ or -] 0.57 *       69

           El-        Biomphalaria    7.53 [+ or -] 0.26 **     130
           Khankak

           Kobry      Biomphalaria   6.42 [+ or -] 0.08 ***      96
           El-        Planorbis       6.24 [+ or -] 0.51 *       91
           Lansh
Dakahlya   Gammalya   Biomphalaria    6.72 [+ or -] 0.40 **     106
           Nasayma    Biomphalaria   13.95 [+ or -] 0.30 ***    327
                      Planorbis      12.66 [+ or -] 0.04 ***    287
                      Physa          6.24 [+ or -] 0.04 ***      91
           Matarya    Biomphalaria    7.95 [+ or -] 0.35 **     143
Damietta   Annanya    Physa            5.1 [+ or -] 0.41 *       56
           Sayala     Planorbis

Parameter                                        Globulin (g/dl)

Treatments                              Mean [+ or -] SD      Change
                                                                %
Control lab                            2.94 [+ or -] 0.11

Bort-      Kaar       Biomphalaria    3.54 [+ or -] 0.11 *      20
  Said     El-Bahr    Planorbis      6.45 [+ or -] 0.04 ***    119

           El-        Biomphalaria    4.89 [+ or -] 0.30 *      66
           Khankak

           Kobry      Biomphalaria     3.87 [+ or -] 0.74       32
           El-        Planorbis      4.62 [+ or -] 0.12 **      57
           Lansh
Dakahlya   Gammalya   Biomphalaria   4.77 [+ or -] 0.12 **      62
           Nasayma    Biomphalaria   9.12 [+ or -] 0.22 ***    210
                      Planorbis      11.61 [+ or -] 0.63 **    295
                      Physa            2.7 [+ or -] 0.15        -8
           Matarya    Biomphalaria     3.72 [+ or -] 0.25       27
Damietta   Annanya    Physa           4.8 [+ or -] 0.16 **      63
           Sayala     Planorbis

Parameter                            A/G Ratio <>

Treatments

Control lab                              1.13

Bort-      Kaar       Biomphalaria       1.93
  Said     El-Bahr    Planorbis          0.85

           El-        Biomphalaria       1.63
           Khankak

           Kobry      Biomphalaria       1.22
           El-        Planorbis          1.34
           Lansh
Dakahlya   Gammalya   Biomphalaria       1.44
           Nasayma    Biomphalaria       1.53
                      Planorbis          1.12
                      Physa              2.35
           Matarya    Biomphalaria       2.16
Damietta   Annanya    Physa              1.05
           Sayala     Planorbis

Parameter                               Total Bilirubin (Umol/l)

Treatments                             Mean [+ or -] SD     Change
                                                              %
Control lab                            2.8 [+ or -] 0.1

Bort-      Kaar       Biomphalaria    4.4 [+ or -] 0.0 *     1.6
  Said     El-Bahr    Planorbis        4.8 [+ or -] 0.8       2

           El-        Biomphalaria
           Khankak

           Kobry      Biomphalaria   6.3 [+ or -] 0.3 **     3.5
           El-        Planorbis       6.5 [+ or -] 1.2 *     3.7
           Lansh
Dakahlya   Gammalya   Biomphalaria   5.3 [+ or -] 0.1 **     2.5
           Nasayma    Biomphalaria    4.5 [+ or -] 0.0 *     1.7
                      Planorbis      10.4 [+ or -] 0.0 **    7.6
                      Physa          14.7 [+ or -] 1.8 *     11.9
           Matarya    Biomphalaria   5.0 [+ or -] 0.1 **     2.2
Damietta   Annanya    Physa           5.7 [+ or -] 0.9 *     2.9
           Sayala     Planorbis        4.8 [+ or -] 0.8       2

Parameter                              Direct Bilirubin (mg/ dl)

Treatments                            Mean [+ or -] SD     Change
                                                             %
Control lab                           0.2 [+ or -] 0.04

Bort-      Kaar       Biomphalaria    0.6 [+ or -] 0.0      200
  Said     El-Bahr    Planorbis       0.1 [+ or -] 0.0      -50

           El-        Biomphalaria
           Khankak

           Kobry      Biomphalaria    0.3 [+ or -] 0.0       50
           El-        Planorbis      1.1 [+ or -] 0.1 **    450
           Lansh
Dakahlya   Gammalya   Biomphalaria    0.1 [+ or -] 0.4      -50
           Nasayma    Biomphalaria   2.5 [+ or -] 0.0 **    1150
                      Planorbis       0.4 [+ or -] 0.0      100
                      Physa           1.8 [+ or -] 1.3      800
           Matarya    Biomphalaria    0.4 [+ or -] 1.5      100
Damietta   Annanya    Physa          2.1 [+ or -] 0.4 *     950
           Sayala     Planorbis       0.3 [+ or -] 0.2       50

Parameter                              In-Direct Bilirubin (U/mg)

Treatments                             Mean [+ or -] SD     Change
                                                              %
Control lab                            2.5 [+ or -] 0.1

Bort-      Kaar       Biomphalaria    3.8 [+ or -] 0.0 *      52
  Said     El-Bahr    Planorbis        4.7 [+ or -] 0.8       88

           El-        Biomphalaria
           Khankak

           Kobry      Biomphalaria   6.0 [+ or -] 0.3 **     140
           El-        Planorbis      5.4 [+ or -] 0.4 **     116
           Lansh
Dakahlya   Gammalya   Biomphalaria   5.1 [+ or -] 0.2 **     104
           Nasayma    Biomphalaria     2.0 [+ or -] 0.0      -20
                      Planorbis      10.0 [+ or -] 0.0 *     300
                      Physa          12.9 [+ or -] 0.6 **    416
           Matarya    Biomphalaria   4.4 [+ or -] 0.2 **      76
Damietta   Annanya    Physa            3.6 [+ or -] 1.3       44
           Sayala     Planorbis        4.5 [+ or -] 0.7       80

*, ** & *** significant compared to control value at p<0.05, p<0.01 &
p<0.001, respectively. <> A/G = Ratio of albumin /globulin
concentration

Table 3: Catalase (CAT), glutathione-S-transferase (GST) and Gamma-
glutamyl transpeptidase (GGT) in tissue extract of snails collected
from Lake Manzala.

Parameter                            CAT (Unites/g)

Treatments                              Mean [+ or -] SD       Change
                                                                 %

                                     Field collected snails

Control lab                            9.06 [+ or -] 0.18

Port-      Kaar       Biomphalaria   3.175 [+ or -] 0.37 **     -65
Said       El-Bahr    Planorbis       15.15 [+ or -] 1.9 *       67

           Kobry      Biomphalaria    3.96 [+ or -] 0.67 **     -56
           El-Lansh   Planorbis        7.59 [+ or -] 0.00       -16

Dakahlya   Gammalya   Biomphalaria     7.92 [+ or -] 1.59       -13
                      Planorbis       16.7 [+ or -] 0.00 *       84
           Nasayma    Biomphalaria     10.69 [+ or -] 1.31       18
                      Planorbis      1.36 [+ or -] 0.25 ***     -85
                      Physa           0.89 [+ or -] 0.00 **     -90
           Matarya    Biomphalaria    7.19 [+ or -] 0.05 **     -21
                      Physa          18.15 [+ or -] 0.00 **     100
                      Planorbis       15.52 [+ or -] 0.00 *      71
Damietta   Annanya    Physa           7.195 [+ or -] 0.54 *     -21
                      Planorbis      25.785 [+ or -] 1.83 **    185
           Sayala     Planorbis      17.31 [+ or -] 0.00 **      91

Parameter                            GST (Unites/g)

Treatments                             Mean [+ or -] SD     Change
                                                              %

                                     Field collected snails

Control lab                           3.07 [+ or -] 0.5

Port-      Kaar       Biomphalaria    1.52 [+ or -] 0.18     -50
Said       El-Bahr    Planorbis      5.60 [+ or -] 0.13 *     82

           Kobry      Biomphalaria    2.11 [+ or -] 0.26     -31
           El-Lansh   Planorbis       4.66 [+ or -] 0.0       52

Dakahlya   Gammalya   Biomphalaria    2.44 [+ or -] 0.33     -21
                      Planorbis       5.31 [+ or -] 0.0       73
           Nasayma    Biomphalaria    3.93 [+ or -] 0.49      28
                      Planorbis      0.83 [+ or -] 0.19 *    -73
                      Physa           0.53 [+ or -] 0.0      -83
           Matarya    Biomphalaria    3.63 [+ or -] 0.72      18
                      Physa           6.63 [+ or -] 0.0      116
                      Planorbis       5.80 [+ or -] 0.0       89
Damietta   Annanya    Physa           4.04 [+ or -] 0.93      32
                      Planorbis      6.71 [+ or -] 0.41 *    119
           Sayala     Planorbis       3.46 [+ or -] 2.7       13

Parameter                            GGT (Unites/g)

Treatments                             Mean [+ or -] SD     Change
                                                              %

                                     Field collected snails

Control lab                            999 [+ or -] 24

Port-      Kaar       Biomphalaria     653 [+ or -] 311      -35
Said       El-Bahr    Planorbis      160 [+ or -] 19 ***     -84

           Kobry      Biomphalaria    1241 [+ or -] 172       24
           El-Lansh   Planorbis       1227 [+ or -] 0 *       23

Dakahlya   Gammalya   Biomphalaria     909 [+ or -] 147       -9
                      Planorbis         984 [+ or -] 0        -1
           Nasayma    Biomphalaria     716 [+ or -] 118      -28
                      Planorbis       1152 [+ or -] 237       15
                      Physa             857 [+ or -] 0       -14
           Matarya    Biomphalaria    1274 [+ or -] 46 *      28
                      Physa             915 [+ or -] 0        -8
                      Planorbis        1056 [+ or -] 0        6
Damietta   Annanya    Physa          7651 [+ or -] 651 **    666
                      Planorbis      3901 [+ or -] 731 *     290
           Sayala     Planorbis       1123 [+ or -] 266       12

*, ** & *** significant compared to control value at p< 0.05, p<0.01
& p<0.001, respectively.

Table 4: Hematologic parameters of snails collected from Lake Manzala.

        Parameters                Total cell count

Examined                             Mean [+ or -] SD      Change
                                                             %

Control                              3.2 [+ or -] 1.0

Port    Kaar       Biomphalaria    2.25 [+ or -] 0.7 *      -30
Said    El-Bahr    Planorbis       1.2 [+ or -] 0.3 ***     -63

        Kobry      Biomphalaria     2.35 [+ or -] 0.6       -27
        El-Lansh   Planorbis      0.95 [+ or -] 0.1 ***     -70

        Matarya    Biomphalaria      2.6 [+ or -] 0.1       -19

Daka-   Gammalya   Biomphalaria    1.4 [+ or -] 0.0 ***     -56
hlya    Nasayma    Biomphalaria    0.9 [+ or -] 0.4 ***     -72
        Sayala     Planorbis       1.95 [+ or -] 0.0 **     -39

Damie   Annanya    Physa            2.65 [+ or -] 0.5       -17
tta                Planorbis      1.63 [+ or -] 0.04 ***    -49

        Parameters                     Hyalinocytes

Examined                          %      Mean [+ or -] SD     Change
                                                                %

Control                           57    1.85 [+ or -] 0.5

Port    Kaar       Biomphalaria   61     1.4 [+ or -] 0.7      -24
Said    El-Bahr    Planorbis      57   0.7 [+ or -] 0.0 ***    -62

        Kobry      Biomphalaria   60   1.35 [+ or -] 0.4 *     -27
        El-Lansh   Planorbis      45   0.4 [+ or -] 0.0 ***    -78

        Matarya    Biomphalaria   71    1.85 [+ or -] 0.2       0

Daka-   Gammalya   Biomphalaria   77   1.1 [+ or -] 0.0 ***    -41
hlya    Nasayma    Biomphalaria
        Sayala     Planorbis      70    1.4 [+ or -] 0.0 *     -24

Damie   Annanya    Physa          70    1.85 [+ or -] 0.6       0
tta                Planorbis

        Parameters                Round small hemocytes

Examined                          %       Mean [+ or -] SD      Change
                                                                  %

Control                           27     0.8 [+ or -] 0.28

Port    Kaar       Biomphalaria   24     0.5 [+ or -] 0.28       -38
Said    El-Bahr    Planorbis      24   0.25 [+ or -] 0.21 ***    -69

        Kobry      Biomphalaria   24     0.55 [+ or -] 0.21      -31
        El-Lansh   Planorbis      41   0.35 [+ or -] 0.07 ***    -56

        Matarya    Biomphalaria   18    0.45 [+ or -] 0.21 *     -44

Daka-   Gammalya   Biomphalaria   16   0.2 [+ or -] 0.00 ***     -75
hlya    Nasayma    Biomphalaria
        Sayala     Planorbis      15    0.3 [+ or -] 0.0 ***     -63

Damie   Annanya    Physa          23     0.55 [+ or -] 0.21      -31
tta                Planorbis

        Parameters                     Granuolocytes

Examined                          %      Mean [+ or -] SD      Change
                                                                 %

Control                           16     0.55 [+ or -] 0.2

Port    Kaar       Biomphalaria   15     0.35 [+ or -] 0.4      -36
Said    El-Bahr    Planorbis      16    0.25 [+ or -] 0.3 *     -55

        Kobry      Biomphalaria   16     0.45 [+ or -] 0.5      -18
        El-Lansh   Planorbis      14   0.20 [+ or -] 0.0 ***    -64

        Matarya    Biomphalaria   11     0.30 [+ or -] 0.3      -45

Daka-   Gammalya   Biomphalaria   7    0.10 [+ or -] 0.0 ***    -82
hlya    Nasayma    Biomphalaria
        Sayala     Planorbis      15    0.3 [+ or -] 0.0 **     -45

Damie   Annanya    Physa          7    0.25 [+ or -] 0.1 **     -55
tta                Planorbis

        Parameters
                                  Hemoglobin (g/100ml)
Examined

Control                              1.8

Port    Kaar       Biomphalaria      2.3           28
Said    El-Bahr    Planorbis         2.6           44

        Kobry      Biomphalaria      1.8           0
        El-Lansh   Planorbis         2.3           28

        Matarya    Biomphalaria      2.0           11

Daka-   Gammalya   Biomphalaria      1.7           -6
hlya    Nasayma    Biomphalaria
        Sayala     Planorbis

Damie   Annanya    Physa             0.8          -56
tta                Planorbis

*, ** & *** significant compared to control value at p<0.05, p<0.01 &
p<0.001, respectively.
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Title Annotation:Research Article; Lake Manzala, Egypt
Author:Khayat, Hanaa M.M. El-; Abdel-Hamid, Hoda; Gaber, Hanan S.; Mahmoud, Kadria M.A.; Flefel, Hassan E.
Publication:Fisheries and Aquaculture Journal
Article Type:Report
Geographic Code:7EGYP
Date:Dec 1, 2015
Words:8093
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