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Response of Spleen and Jejunum of Mice Infected with Schistosoma mansoni to Mulberry Treatment.

Byline: Amira A. Bauomy, Mohamed A. Dkhil, Marwa S.M. Diab, Omar S.O. Amer, Rafat M. Zrieq and Saleh Al-Quraishy

: Abstract.- Schistosomiasis is the second most predominant tropical disease in Africa after malaria. In the developing world, it has a great public health and socio-economic importance. Here, we aimed to assess the antioxidant and anti-schistosomal activities of Morus alba leaves (MLE) methanolic extract (200, 400 and 800 mg/kg) on the noticed tissue damage caused by Schistosoma mansoni infection in mice. The infection resulted in marked histopathological abnormalities in the spleen and jejunum. Moreover, infection induced splenomegally and the spleen appeared with disorganized red and white pulps while the jejunum of the infected mice appeared with some inflammation, vacuolation of the epithelium, and destruction of some villi. Also, the number of goblet cells within the infected villi was significantly increased. In addition, schistosomiasis caused oxidative damage where the level of glutathione (GSH) was reduced significantly while the levels of malondialdehyde (MDA) and nitrite/nitrate were elevated significantly. On the other hand, oral gavage of MLE extract ameliorated the tissues damage and oxidative stress induced by Schistosomasis. The present study indicates that MLE extract possess a highly promising ameliorative effect against histopathological damages and oxidative stress induced by Schistosomasis.

Keywords: Schistosoma mansoni, Morus alba, oxidative stress, glutathione level. INTRODUCTION

Helminth parasites of the genus Schistosoma are the causative agents of schistosomiasis, which is a neglected disease, so it remains a significant public health problem in tropical and subtropical regions (Quack et al., 2006; Steinmann et al., 2006). In Egypt, the disease is well established and it is estimated that up to 70% of the rural population in endemic areas is affected (Al Sherbiny et al., 2003).The massive egg production of schistosomes is leading to granuloma formation in the gut, intestine, bladder, spleen, liver and lungs (Ross et al., 2002; AraAjo et al., 2010), and a substantial number of eggs are trapped in the liver and intestine(Helmy et al., 2009). The intestine or urinary system bleeding, liver and spleen enlargement are the most common pathological changes found in chronic schistosomiasis (Burke et al., 2009).In recent decades, there has been a growing interest to search for extracts and pure compounds, especially those derived from plants that exhibit potential schistosomicidal properties. This is as one alternative method to the conventional chemical control, particularly in the absence of a vaccine and the probability of drug resistance (Ndamba et al.,1994; McManus and Loukas, 2008).Morus alba (Moraceae) is a white mulberry,and it has many medicinal properties so it has been used since ancient times in folk medicine (Nade et al., 2009). M. alba has been used for ailments of respiratory system, as well as, edema, wound healing and diabetes. It has been reported that M. alba have antibacterial, neuroprotective, hypolipidemic and hypotensive activities (Chai et al., 2005; Kang, 2006; Yadav et al., 2008).A number of earlier investigations indicated that M. alba exhibits an antioxidant effect due to the presence of phenolic compounds and some vitamins which act as a good source of natural antioxidants (Fukai et al., 2003). The current study was aimed at investigating the antioxidant potential role of M. alba in reducing oxidative stress in the spleen and jejunum of mice infected with S. mansoni.


AnimalsFifty Swiss albino mice were bred underspecified pathogen-free conditions and fed a standard diet and water ad libitum. The experiments were performed only with male mice at an age of 9 to 11 weeks and were approved by state authorities and followed the Egyptian rules for animal protection.

Preparation of Morus alba leaves extract (MLE)Leaves of Morus alba plant were collected from mulberry trees which cultivated in El-Maadi, Cairo governorate, identified by the Department of Botany, Faculty of Science, Helwan University, dried at a temperature not exceeding 40oC and powdered. The investigated dried powdered leaves were separately extracted with 70% methanol. The methanolic plant extract was filtered and evaporated to dryness in vacuo at a temperature not exceeding50oC. The dried plant extract was kept in dark bottle for investigation. According to Kalantari et al. (2009) three doses 200, 400 and 800 mg/kg bodyweight were prepared by dissolving in distilledwater (Alam et al., 2002).

Schistosoma mansoni infectionS. mansoni cercariae were obtained from Schistosome Biological Supply Center at Theodor Bilharz Research Institute, Imbaba, Giza, Egypt. Mice were exposed to 8010 S. mansoni cercariae per mouse by the subcutaneous injection method, modified by Oliver and Stirewalt (1952).

Experimental designFive groups, each of ten mice, were used in this study. First group (-MLE) was non-infected and served as a vehicle control (uninfected) group. It received 100 l water/mouse orally for 10 days. After 46 days post infection (p.i.) with 8010 S. mansoni cercariae, infected animals were divided into the remaining four groups, the second group is infected (-MLE) group. The 3rd, 4th and 5th groups were infected with S. mansoni. Thereafter, the infected animals of these groups, received orally200, 400 and 800 mg/kg body weight of MLE, respectively, once daily for 10 days.

Preparation of spleen and jejunum tissuesOn day 56 p.i. with S. mansoni and MLE administration, the animals of all groups were decapitated. Spleen and jejunum were removed, weighed and rapidly cut into smaller pieces. A few pieces were fixed in 10% neutral buffered formalin for histopathological investigations, while others were homogenized in ice-cold medium containing50 mM TrisHCl and 300 mM sucrose, pH 7.4 (Tsakiris et al., 2004) and finally stored at -80C until use in the various biochemical determinations.

Spleen indexAt the end of the experimental period, each mouse was weighed; the spleen was removed and weighed. Finally, the spleen index was calculated (ratio of spleen weight in mg/mouse to body weight in g/mouse).

HistopathologyFormalin-fixed spleen and jejunum wereembedded in paraffin, and 5 m sections were stained with hematoxylin and eosin. Mice jejuna were stained with Alcian blue for the identification of the goblet cells. For each animal, the number of goblet cells in the jejunum was counted on at least ten well-orientated villous crypt units (VCU). Results were expressed as the mean number of goblet cells per ten VCU (Allen et al., 1986).

Estimation of the reduced glutathione (GSH) levelGSH level in spleen and jejunum was determined by the methods of Ellman (1959). The method is based on the reduction of Ellman's reagent (5, 5'dithiobis (2-nitrobenzoic acid) "DTNB") with GSH to produce a yellow compound. The reduced chromogen is directly proportional to GSH concentration and its absorbance can be measured at 412 nm.Determination of nitrite/nitrate and malondialdehyde (MDA) levelsThe nitrite/nitrate and MDA levels weredetermined according to Green et al. (1982) andOhkawa et al. (1979), respectively.

Statistical analysisThe obtained data were presented as means standard error. One-way ANOVA was carried out, and the statistical comparisons among the groups were performed with Duncan's test using a statistical package program (SPSS version 17.0). P= 0.001 was considered as significant for allstatistical analysis in this study.


S. mansoni resulted in a highly significant increase in splenic index (ratio of spleen weight in mg/mouse to body weight in g/mouse) (Fig. 1). Oral gavage of methanolic extract of M. alba leaves (MLE) to infected mice reduced the index significantly. The maximum effect of MLE extract was at a dose of 200 mg/kg that showed a complete recovery in the splenic index indicating its ameliorative effect on schistosomiasis.

The normal spleen was composed of white and red pulps surrounded by a capsule of dense connective tissue (Fig. 2). The white pulp was composed of a central, T-cell rich zone, and a peri- arterial lymphoid sheath surrounded by B-cell-rich primary follicles. The white pulp was separated from the red pulp by the marginal sinus embedded in a layer of marginal zone lymphocytes. On day 55 post-infection with S. mansoni, the white pulp enlarged due to cellular proliferation. The limit between white and red pulp started to disappear (Fig. 2), and the spleen increased in size. Vacuolation of some splenic cells was detected. Most of the cells were darkly stained and the sinusoidal spaces were large. The histological lesion is still present after treatment of mice with M. alba but the tissue is much improved after treatment with the dose of 800 mg/kg.Histopathological examination of the intestine of the infected non-treated mice revealed also chronic inflammation and numerous large granulomas in the mucosa, submucosa and in some instances penetrating the muscular layer. In most instances, a plenty of granulomas with central egg trapped could be seen (Fig. 3). In Morus alba treated groups, the intestine showed apparent amelioration where there were fewer and non- developed granulomas. In most cases, there were few eggs without concentric fibrosis (Fig. 3). Moreover, infection of mice with S. mansoni was able to significantly increase the number of goblet cells (Fig. S1, Fig. 4). This number was increased more than 2 fold compared to the non-infected control mice. M. alba could reduce the increased number of goblet cells specially when mice were treated with a dose of 400 mg/kg (Fig. 4).Data in Table I showed that the infected micewith S. mansoni decreased the level of GSH in selected organs under investigation (spleen and jejunum). Gavage of the three doses of MLE to S. mansoni infected mice was able to increase the GSH level in both organs when compared to the infected mice.

Fig. 1. Morus alba induces changes in spleen index of mice infected with S. mansoni. Values are Means SE.aRatio of spleen weight in mg/mouse to body weight in g/mouse. The nitrite/nitrate level was raisedsignificantly (P=0.001) as a result of schistosomiasis in spleen and jejunum versus non-infected group (Table I). The ameliorative effect of MLE was noticed in infected mice at the different doses.In spleen the most effective dose was 200 mg/kg, while, 400 and 800 mg/kg induced recovery in jejunum.Similarly, S. mansoni infection to mice resulted in a highly significant increment of MDA level in spleen and jejunum at P=0.001 as compared to the control group as shown in Table I. Treatment of the schistosome infected mice with MLE induced a highly significant reduction of MDA level in spleen, the maximum effect was recorded at a dose of 400 mg/kg. Moreover, the most effective dose of M. alba extract in jejunum was 200 mg/kg.


The spleen index in the present work showed a highly significant increment as a result of schistosomal infected mice. Our findings were in agreement with Soomro et al. (2001), Silva-Souza and Vasconcelos (2005), da Silva et al. (2012) and CorrAa et al. (2013). Also, Soomro et al. (2001) and CorrAa et al. (2013) noticed that splenomegaly is prominent in S. mansoni where, the schistosome infection resulted in a highly significant increment in the total spleen weights of infected mice (da Silva et al., 2012). In addition, Silva-Souza and Vasconcelos (2005) indicated that S. mansoni

Table I.-###Effect of M. alba leave extracton glutathione (GSH), nitrate/nitrite and lipid peroxidation level as expressed by

###malondialdehyde (MDA) equivalents in splenic and intestinal homogenates of S. mansoni infected mice.

###Infected + Treated with M. alba extract


###200 mg/Kg###400 mg/Kg###800 mg/Kg

GSH (mg/g)

###Spleen###49.162.69###26.141.78 a###27.241.25 a###29.192.36 a###27.770.72 a

###Intestinal###06.060.29###05.050.98###07.450.39###6.480.40###10.941.48 ab

Nitrite/nitrate (mol/g)

###Spleen###51.861.99###81.672.61 a###57.922.24 b###55.021.67 b###50.111.40 b

###Intestinal###118.91.70###280.02.66 a###102.12.27 ab###130.02.33 ab###116.32.43 b

MDA (nmol/g)

###Spleen###99.311.98###125.62.02 a###84.510.99 ab###80.420.80 ab###113.32.19 ab

###Intestinal###05.790.98###20.631.77 a###08.941.58 b###19.931.60 a###13.891.62 ab

histopathology is characterized by the presence of granuloma with parasitic eggs, with an increase in the size of the spleen. In addition, our results cleared that the treatment with MLE reduced the spleen index in S. mansoni infected mice, where the most effective dose is 200 mg/kg. Schistosomiasis mostly; affecting the intestine causing granuloma formation (El Banhawey et al., 2007; Riad et al.,2008). Mature S. mansoni are depositing eggs in theintestinal wall that either pass to the gut lumen and are expelled in the faeces or travel to the liver (Gryseels et al., 2006). Eggs release antigens that produce varying degrees of granulomatous response in the intestines of the definitive host (Hirata et al.,1993).Riad et al. (2008) reported that, granulomas were evident in the subserosa, muscularis and submucosa. Besides, an apparent increase of goblet cells number, per villus was recorded. All these results were cleared in the infected non-treated mice of our investigation. Otherwise, the infected mice treated with MLE showed fewer and non-developed granulomas in the intestinal tissue and in most cases, there were few eggs without concentric fibrosis. In addition, it reduced the increased number of goblet cells; indicating to the antifibrotic and anti-inflammatory roles of M. alba leaves (Choi and Hwang, 2005; Amer et al., 2013).The extent of granuloma formation and egg deposition in the tissues determine the severity of the disease. Moreover, an imbalance between pro-and anti- oxidant processes has been demonstrated both in vitro (Feldman et al., 1990) and in vivo (Gharib et al., 1999).S. mansoni induced a highly significantreduction in GSH level in spleen and jejunum, which indicates that schistosomiasis causes more liberation of free radicals. On the other hand, MLE gavage to S. mansoni infected mice resulted in highly significant increment in GSH level of spleen and jejunum. Our results are in agreement with the observation of (El Sokkary et al., 2002; Amer et al.,2013; Diab et al., 2013; de Oliveira et al., 2013).de Oliveira et al. (2013) reported that the non-enzymatic antioxidant capacity in spleen were decreased as a result of schistosome infection. El- Sokkary et al. (2002) concluded that there were reductions in glutathione, superoxide dismutase, and vitamin E in the spleen of S. mansoni infected mice. In addition, the level of GSH was increased as a result of treatment of infected mice with an antioxidant. Likewise, Amer et al. (2013) and Diab et al. (2013) speculated that Morus alba leaves extract gavage to infected mice resulted in a highly significant increment of GSH level.In the current investigation, evidence of increased nitrite/nitrate and MDA levels in spleen and jejunum of S. mansoni infected mice was seen. On the contrary, the treated S. mansoni infected mice with MLE caused a highly significant decrease in nitrite/nitrate and MDA levels of the studied organs which are in agreement with El Sokkary et al. (2002), Amer et al. (2013) and Diab et al. (2013).Raso et al. (2001) and El Sokkary et al. (2002) deduced that the spleen oxidative stress was prompted by S. mansoni infection. Our data revealed that the nitrite/nitrate and MDA levels of spleen were increased significantly in schistosoma- infected mice were dead by 56 day post-infection. In addition, the main organ affected during the course of the pathology, the spleen, was shifted to a pro- oxidant state (La Flamme et al., 2001; de Oliveira et al., 2013). The imbalance of oxidative parameters may be due to the egg deposition, changes in vascular tone and soluble immune mediators (Wynn et al., 2004; Pearce, 2005).In the acute and chronic stages of S. mansoni infection, both structural and functional changes occur in the intestine of infected mice (Bogers et al.,2000). The chronic infection of mice with S. mansoni severely disturbs the gastrointestinal motility. This is characterized by a hypercontractile activity of the small intestine in the chronic stages of infection and by a disturbed transit time of a semi-liquid meal through the small intestine (Bogers et al., 2000; Moreels et al., 2001). Granulomatous tissue causes the loss of elasticity in the intestinal wall and as the disease progresses the tissue can become calcified (Warren, 1982).El Sokkary et al. (2002) speculated that the oxidative stress that generated in the spleen due to schistosomiasis was reduced by an antioxidant. Amer et al. (2013) and Diab et al. (2013) observed that M. alba treatment prevented the increase in nitrite/nitrate and MDA, probably in part by scavenging the very reactive components. The MLE contain triterpenes (lupeol), sterols (AY-sitosterol), bioflavonoids (rutin, moracetin, quercetin-3- triglucoside and isoquercitrin), coumarins, volatile oil, alkaloids, amino acids and organic acids (Doi et al., 2001).Collectively, all the mentioned changes in the spleen and jejunum pathology induced a state of oxidative stress in infected mice with S. mansoni and this stress was significantly reduced by MLE treatment indicating to its antioxidant properties and antischistosomal activity. ACKNOWLEDGMENT

The authors extend their appreciations to the Deanship of Scientific Research at King Saud University for funding the work through the research group project no. RGP-198.


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Author:Bauomy, Amira A.; Dkhil, Mohamed A.; Diab, Marwa S.M.; Amer, Omar S.O.; Zrieq, Rafat M.; Al-Quraishy
Publication:Pakistan Journal of Zoology
Article Type:Report
Geographic Code:7EGYP
Date:Jun 30, 2014
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