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Schistosomicidal, hepatoprotective and antioxidant activities of the methanolic fraction from Clerodendrum umbellatum Poir leaves aqueous extract in Schistosoma mansoni infection in mice
© Jatsa et al. 2015
Received: 31 January 2015
Accepted: 21 July 2015
Published: 24 July 2015
The intensive use of Praziquantel for the treatment of schistosomiasis has raised concerns about the possible emergence of drug-resistant schistosomes. As drug treatment is an important feature of schistosome control programs, the search for alternative drugs is therefore a priority. The aim of this study was to assess the schistosomicidal, hepatoprotective and antioxidant activities of the methanolic fraction from Clerodendrum umbellatum Poir leaves aqueous extract.
A phytochemical screening of the fraction of C. umbellatum was conducted. The fraction was administered orally and daily to Schistosoma mansoni-infected mice (BALB/c) from the 36th day post-infection for 28 days at 100, 200 and 400 mg/kg. Praziquantel (500 mg/kg) was used as reference drug. Non-infected and infected-untreated mice served as controls. All mice were sacrificed at 65th day post-infection. Body weight, liver/body and spleen/body weights, as well as worm burden, fecal egg count, liver and intestine egg load were determined. In the plasma, levels of total protein, transaminases (ALT, AST), alkaline phosphatase and total bilirubin were monitored to assess the possibility of liver damage. Malondialdehyde (MDA), catalase (CAT) and glutathione (GSH) levels were measured in the liver as biomarkers of the oxidative stress.
The phytochemical analysis of the fraction from C. umbellatum aqueous leaves extract revealed the presence of alkaloids, flavonoids, cardiac glycosides, phenols, saponins, tannins and terpenoids. The worm burden, fecal egg count and egg load in the liver and intestine of infected mice treated with the fraction were significantly (p < 0.001) fewer than in infected-untreated mice. Only the highest-fraction dose reduced the worm and egg burdens in a similar way as praziquantel. Hepatosplenomegaly induced by S. mansoni infection was reduced by the treatment. The liver function on infected mice was ameliorate after administration of the fraction by significant reduction of ALT activity (35.43 to 45.25 %) and increase of total protein level (44.79 to 70.03 %). The methanolic fraction of C. umbellatum prevents the elevated MDA level induced by the infection while significant increase in catalase activity (297.09 to 438.98 %) and glutathione level (58.23 to 95.88 %) were observed after treatment.
This study disclosed the schistosomicidal, hepatoprotective and antioxidant activities of the methanolic fraction from C. umbellatum leaves aqueous. These fraction’s activities were similar to those of praziquantel. This fraction can be considered as a promising source for schistosomicidal agents.
KeywordsClerodendrum umbellatum Liver function Antioxidants Oxidative stress Schistosoma mansoni
Schistosomiasis is a chronic and debilitating disease affecting more than 200 million people in tropics and subtropics, with 97 % of them living in Africa . The chronic and debilitating nature of the disease has resulted in heavy expenditure in public health and economic productivity in developing countries, and has prompted the initiation of large scale control programs . Schistosoma mansoni infection is characterized by the embolization of eggs from the intestine to the liver through the portal system. Most pathology in schistosomiasis is then attributed to the host reaction to the eggs. The toxic egg material destroys the host tissue cells and the antigenic material stimulates the development of large inflammatory reactions around the egg. At the site of inflammation, oxidative stress occurs and lead to the generation of free radicals and the reduction of endogenous antioxidants [3, 4]. Presently, there is no available vaccine against schistosomiasis and the current treatment relies on praziquantel. However, praziquantel does not treat early infection or prevent reinfection . In addition to, numerous evidences indicate the emergence of Schistosoma mansoni strains resistant to praziquantel [6, 7]. Therefore, there is growing consensus that novel antischistosomal drugs should be discovered and developed . During Schistosoma mansoni infection, mice are good definitive host and their behavior is similar to that of humans. Thereby, the mouse is the animal of choice for in vivo antischistosomal drug screening . In view to search complementary and/or alternative therapy for schistosomiasis, many studies on traditional medicinal plants have been conducted [10–15]. Previous ethnobotanical surveys revealed common use of plant materials in Africa for the treatment of intestinal helminthiasis. In Cameroon, the leaves of Clerodendrum umbellatum Poir (Labiateae) are among the common medicinal plants used by traditional healers to treat intestinal helminthiasis . Our previous study has established the antischistosomal activity of C. umbellatum leaves aqueous extract . The present study was carried out to evaluate the schistosomicidal, hepatoprotective and antioxidant activities of the methanolic fraction from C. umbellatum leaves aqueous extract on Schistosoma mansoni infected mice.
Plant material, extraction and fractionation
Clerodendrum umbellatum was collected in April 2012 at the locality of Mekok, near Sangmelima in the South region of Cameroon. The plant was identified at the National Herbarium of Yaoundé, Cameroon in comparison with the specimen 7405 SRF/Cam and conserved under the voucher N° 7405.
Leaves were dried in the shade, powdered and mixed with water (100 g/L) for 24 h of maceration at room temperature. The solution was filtered, frozen and then lyophilized to obtain the aqueous extract, with a recovery rate of 17 %. The aqueous extract (120 g) was fractionated by liquid–liquid partition with solvents of increasing polarity: n-hexane, ethyl acetate and methanol. Solvents were removed in a rotatory evaporator, at maximum temperature of 40 °C. This process allowed obtaining 31.57 g of a methanolic fraction.
The methanolic fraction from C. umbellatum leaves aqueous extract was subjected to qualitative chemical tests to identify phytochemical constituents in the fraction. The screening of alkaloids, anthraquinones and cardiac glycosides was performed by the Mayer’s test, the Bornträger’s test and the Keller-Killiani’s test respectively. Ferric chloride test (FeCl3) was used for the identification of phenols and tannins, Fehling’s test for reducing sugars, foam test for saponins and Liebermann-Burchard’s test for steroids and triterpenes. The presence of flavonoids, lipids and terpenoids was performed using the ammonia test, the grease spot test and the Salkowski’s test respectively .
Animals and infection
Eight weeks old BALB/c mice from the animal house of the “Centre for Schistosomiasis and Parasitology” of Yaoundé–Cameroon, weighing 20–25 g were used in this study. They were housed in polypropylene cages in a bioterium under natural 12 h light/12 h dark cycles, temperature maintained between 22 and 25 °C and humidity between 60 and 70 %. Mice were fed with rodents’ diet (flour of corn, wheat, dried fish and roasted soybeans, cotton oil, mineral and vitamins mixture) and water ad libitum. We decided to work with BALB/c mice because they are susceptible to S. mansoni infection . Mice were individually infected with 50 cercariae of S. mansoni (Cameroonian strain) using the method of tail and legs immersion. In brief, mice were first put in contact with water to stimulate urination and defecation. After that, the tail and hind legs of each mouse were immersed for 1 h in water containing 50 cercariae. Cercariae were released from Biomphalaria pfeifferi snails, collected from the river Afeme (Yaoundé, Cameroon) and maintained in the laboratory under standardized conditions.
All procedures in this study followed the ARRIVE guidelines (Animal Research: Reporting In Vivo Experiments) and were approved by the Animal Ethical Committee of the Laboratory of Animal Physiology of the Faculty of Sciences, University of Yaoundé I–Cameroon.
A total of 35 mice were used: 5 healthy mice (NIC group) and 30 S. mansoni-infected mice randomly divided into 5 groups of 6 mice each. Treatment started at the 36th day post-infection and the extract or praziquantel dissolved in distilled water was given by the oral route. Non-infected mice (NIC group) and infected-untreated mice (IC group) received distilled water during 28 consecutive days. The positive control group (PZQ group) received praziquantel at the dose of 500 mg/kg (100 mg/kg/day for 5 days, followed by distilled water for 23 days). Others infected mice were treated with the methanolic fraction from C. umbellatum leaves aqueous extract respectively at the doses of 100 (CuF100 group), 200 (CuF200 group) and 400 mg/kg (CuF400 group) during 28 consecutive days. This period of treatment was chosen according to the prescription of traditional healers and the choice of doses was done on the basis of our previous findings . All animals were sacrificed on the 65th day post-infection.
Measurement of body and organs weights and collection of specimens
During the course of the experiment, each mice was weighed once a week in order to assess body weight variation between pre-infection and post-infection at 65th day. The percentage of weight gain was calculated as follows: P = [(We − Wi)/We] × 100; where P is the percentage of weight gain, We is the body weight at post-infection and Wi is the body weight at pre-infection.
Fecal samples were collected from each mouse before sacrifice and processed for eggs counting. Blood from each animal was collected in the retro-orbital sinus and after centrifugation at 3500 rpm for 15 min, plasma were immediately stored at −70 °C until biochemical analyses were performed. Mice were sacrificed by cervical dislocation and after worm recovery, liver and spleen were removed from each mouse, weighed and their relative weights (g of organ/100 g of body weight) were calculated. The left lobe of the liver and the entire intestine were used to assess egg load while the right lobe of the liver was used for the assessment of hepatic oxidative stress.
Immediately after sacrifice on the 65th day post-infection, mice were perfused in order to recover worms from mesenteric and hepatic veins . The percentage of reduction in worm number was calculated using the method of Tendler et al.  as follows: P = [(C − V)/C] × 100; where P is the percentage of reduction, C is the mean number of worms recovered from infected-untreated mice and V is the mean number of worms recovered from infected-treated mice.
Eggs count in feces, intestine and liver
Feces were weighed, homogenized in 10 % buffered formaldehyde, and stored at 4 °C. Two aliquots of 100 μL each were counted on light microscope. The liver and the intestine which was previously cleaned up and weighed, were digested separately in 4 % KOH solution at 37 °C for 6 h. After digestion, tissue suspensions were centrifuged at 1500 rpm for 5 min and supernatants removed. After three cycles of washing and centrifugation, the number of eggs was determined in two aliquots of 100 μL each using light microscope. Results were expressed in terms of mean number of eggs per gram of feces or per gram of tissue for intestine and liver .
The right lobe of the liver was homogenized in Tris–HCl 50 mM buffer. Homogenates were centrifuged at 3500 rpm for 25 min at 4 °C and supernatants were stored at −70 °C for the determination of some oxidative stress biomarkers.
Liver function tests
In view of evaluating the impact of the treatment with the methanolic fraction of C. umbellatum on the liver function of S. mansoni-infected mice, some parameters were measured in the plasma on the 65th day post-infection.
Plasma level of total proteins was determined using the method of Biuret described by Gornall et al. . Biuret reagent was added to 10 μL of plasma from different mice groups and the developed purple color was measured after 5 min at 540 nm against a blank. The amount of protein was calculated from a standard curve using serial concentration of bovine serum albumin (0.25–1.5 mg/mL).
Alanine aminotransferase (ALT) and aspartate aminotransferase (AST) are known to be indicators of liver injuries. Their activities were determined by the Reitman and Frankel method  using Bioclin kits (Belo Horizonte, Brasil). ALT and AST were measured by monitoring the concentration of pyruvate hydrazone or oxaloacetate hydrazone formed with 2,4-dinitrophenylhydrazine, the color of which is read at 505 nm.
Alkaline phosphatase was estimated by the method of Tietz et al.  using Inmesco kit (Wied, Germany). A mixture of p-nitrophenylphosphate (16 mmol/L), 2-amino-2-methyl-1-propanol (0.9 mol/L), magnesium sulfate (1.6 mmol/L), zinc sulfate (0.6 mmol/L) and HEDTA (2 mmol/L) was used as the working solution. The decrease in absorbance was measured at 410 nm at 1 min intervals for 3 min.
Total bilirubin was assayed according to the protocol described by the Inmesco kit (Wied, Germany). In brief, 100 μL of sulfanilic acid + hydrochloric acid was added to a tube, followed by 20 μL of sodium nitrite, 400 μL of caffeine + sodium benzoate and 100 μL of the plasma. The contents were homogenized and allowed to stand for 5 min. The red color developed after the reaction of bilirubin with sulfanilic acid was read at 546 nm against a blank.
Lipid peroxidation, glutathione status and catalase activity determination
Using murine model of schistosomiasis, it has been demonstrated that S. mansoni induces hepatic oxidative stress due to the production of reactive oxygen species and the reduction of the antioxidant defense processes of the organs [3, 4]. The impact of the treatment of S. mansoni-infected mice with the methanolic fraction of C. umbellatum on their hepatic oxidative stress was then assessed on the 65th day post-infection.
Lipid peroxidation was estimated by determining malondialdehyde (MDA). 250 μL of 20 % trichloroacetic acid and 500 μL of 0.67 % thiobarbituric acid were added to 500 μL of the supernatant,. The tubes were boiled in a water bath at 90 °C for 10 min. After cooling on ice-cold water, the mixture was centrifuged at 3000 rpm for 15 min. The optical density was measured at 530 nm against an appropriate blank . The concentration of MDA was calculated using a molar extinction coefficient of 1.56 × 105 mmol−1 cm−1 and results expressed as nmol/g of liver.
Reduced glutathione (GSH) was assayed following the method described by Ellman . 1500 μL of Ellman reagent (5 mg of 2, 2-dithio-5, 5-nitrobenzoic acid + 250 mL phosphate buffer) was added to 100 μL of the supernatant,. The mixture was shaken and kept for 60 min. Optical density was measured at 412 nm against a blank. The concentration of GSH was calculated using a molar extinction coefficient of 13,600 mol−1 cm−1 and results expressed as μmol/g of liver.
The reaction for assaying catalase activity as described by Sinha , was initiated by adding 187.5 μL of phosphate buffer to 12.5 μL of the supernatant. The reaction started when 50 μL of H2O2 50 mM was added to the mixture and stopped by adding 500 μL of dichromate-acetic acid mixture (50 mL of potassium dichromate 5 % dissolved in 150 mL of glacial acetic acid). Standards tubes were prepared using a solution of H2O2 50 mM. The optical density was recorded at 570 nm. Catalase activity was calculated from the standard curve and expressed as mmol/min/g of liver.
All data were expressed as mean ± standard error of mean (SEM). Statistical differences between controls and experimental groups were assessed by one-way analysis of variance (ANOVA) followed by Newman-Keuls multiple comparison test. P values less than 0.05 (p < 0.05) were considered to be significant. Analysis was performed using GraphPad Prism version 4.00 for Windows (GraphPad Software, San Diego, USA).
Results and discussion
Phytochemical analysis of the methanolic fraction from Clerodendrum umbellatum leaves aqueous extract
The qualitative phytochemical analysis of the methanolic fraction from C. umbellatum leaves aqueous extract revealed the presence of alkaloids, flavonoids, cardiac glycosides, phenols, saponins, tannins and terpenoids. Except phenols, those compounds have previously been found in C. umbellatum aqueous extract .
Effect of the methanolic fraction from Clerodendrum umbellatum leaves aqueous extract on the body weight
Effect of the methanolic fraction from Clerodendrum umbellatum leaves aqueous extract on the body weight of mice at pre-infection and on the 65th day post-infection
Number of animals (n)
Body weight (g)
Weight gain (%)
Pre-infection (1st day)
Post-infection (65th day)
19.30 ± 0.83
24.23 ± 1.05
29.53 ± 2.04 (24.28–34.78)
23.51 ± 0.90
24.31 ± 0.80
3.97 ± 3.87 (−5.50–13.44)
21.22 ± 1.04
26.00 ± 0.98
22.89 ± 2.89 (15.47–30.31)
23.55 ± 0.55
28.14 ± 0.85
19.54 ± 2.56 (12.95–26.12)
21.04 ± 0.89
24.94 ± 1.03
18.60 ± 1.43 (14.93–22.26)
22.74 ± 0.51
27.07 ± 0.74
19.06 ± 1.96 (14.03–24.09)
Effect of the methanolic fraction from Clerodendrum umbellatum leaves aqueous extract on the liver and spleen weights
Effect of the methanolic fraction from Clerodendrum umbellatum leaves aqueous extract on the liver and spleen weights of mice on the 65th day post-infection
Number of animals (n)
Weight (g/100 g)
Weight (g/100 g)
6.23 ± 0.34
0.50 ± 0.04
9.21 ± 0.37
1.45 ± 0.17
6.57 ± 0.46
0.43 ± 0.08
7.68 ± 0.28
0.77 ± 0.08
7.90 ± 0.48
0.79 ± 0.03
5.96 ± 0.47
0.66 ± 0.10
Effect of the methanolic fraction from Clerodendrum umbellatum leaves aqueous extract on worm burden and egg load
Effect of the methanolic fraction from Clerodendrum umbellatum leaves aqueous extract on the liver function
Effect of the methanolic fraction from Clerodendrum umbellatum leaves aqueous extract on some parameters of the liver function of mice on the 65th day post-infection
Number of animals (n)
266.28 ± 9.90
746.07 ± 59.86
391.66 ± 31.85
408.49 ± 36.27
420.52 ± 26.68
481.76 ± 47.09
167.84 ± 10.55
234.23 ± 14.58
168.13 ± 13.41
234.52 ± 23.74
248.24 ± 20.11
261.75 ± 16.25
19.02 ± 2.87
8.04 ± 2.88
20.68 ± 3.24
13.10 ± 2.90
18.38 ± 2.86
20.33 ± 4.07
Total proteins (mg/mL)
4.43 ± 0.22
3.17 ± 0.29
4.73 ± 0.15
4.88 ± 0.18
5.39 ± 0.18
4.59 ± 0.16
Total bilirubin (μmol/L)
19.34 ± 1.71
23.15 ± 1.80
15.32 ± 1.76
16.87 ± 3.78
20.84 ± 1.50
25.59 ± 3.88
Effect of the methanolic fraction from Clerodendrum umbellatum leaves aqueous extract on some markers of oxidative stress
This study showed that the methanolic fraction from Clerodendrum umbellatum leaves aqueous extract exhibits schistosomicidal, hepatoprotective and antioxidant activities in Schistosoma mansoni infection. These activities are probably related to bioactive compounds present in the fraction. Schistosomicidal activity similar to that of praziquantel was displayed by the highest dose of the fraction. Therefore, this fraction could be used as a starting point for the development of phytomedicines and/or source of new molecules against schistosomiasis.
This study was supported by the International Foundation for Science (IFS), grant F/3622-2F awarded to Hermine Boukeng Jatsa.
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