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Advances in Natural and Applied Sciences, 7(5) December 2013, Pages: 519-525
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Antihyperglycemic activities of leaves of Brassica oleracea, Centella asiatica and
Zizyphus mauritiana: Evaluation through oral glucose tolerance tests
Sadia Haque, Tania Naznine, Mohammad Ali, Tania Tabassum Azad, Md. Tanvir Morshed, Nusrat Anik
Afsana, Ishtiaq Ahmed, Mohammed Rahmatullah
Faculty of Life Sciences, University of Development Alternative, Dhanmondi, Dhaka-1205, Bangladesh.
ARTICLE INFO
Article history:
Received 14 November 2013
Received in revised form 24 December
2013
Accepted 28 December 2013
Available online 15 February2014
Key words:
Brassica oleracea, Centella asiatica,
Zizyphus
mauritiana,
antihyperglycemic, OGTT
ABSTRACT
The antihyperglycemic potentials of methanolic extract of leaves of Brassica oleracea,
Centella asiatica, and Zizyphus mauritiana were evaluated by oral glucose tolerance
tests in glucose loaded Swiss albino mice. At doses of 50, 100, 200 and 400 mg per kg
body weight, administration of extract of Brassica oleracea leaves led to reductions in
blood glucose levels in glucose-loaded mice by, respectively, 22.4, 24.2, 34.0, and
47.6%. The results were both dose-dependent, as well as statistically significant. At the
afore-mentioned four doses, administration of extract of leaves of Centella asiatica led
to dose-dependent and significant reductions in blood glucose levels in mice by 29.4,
32.8, 33.6, and 35.7%, respectively. At the same four doses, administration of extract of
leaves of Zizyphus mauritiana lead to dose-dependent and significant reductions in
blood glucose levels by 37.8, 38.9, 40.5, and 43.1%, respectively. A standard
antihyperglycemic drug, glibenclamide, when administered at a dose of 10 mg per kg
body weight, led to reductions in blood sugar levels in glucose-loaded mice within a
range of 41.3 – 54.2%. It can be concluded that the leaves of all three plants possess
significant antihyperglycemic effects and can be utilized as potential sources for new
antidiabetic drugs, or used as crude remedies for lowering of blood sugar in diabetic
patients.
© 2013 AENSI Publisher All rights reserved.
To Cite This Article: Sadia Haque, Tania Naznine, Mohammad Ali, Tania Tabassum Azad, Md. Tanvir Morshed, Nusrat Anik Afsana,
Ishtiaq Ahmed, Mohammed Rahmatullah., Antihyperglycemic activities of leaves of Brassica oleracea, Centella asiatica and Zizyphus
mauritiana: Evaluation through oral glucose tolerance tests. Adv. in Nat. Appl. Sci., 7(5): 519-525, 2013
INTRODUCTION
Brassica oleracea L. var. gongylodes (Family: Cruciferae; English: kohlrabi; Bengali: ol kopi) is a winter
crop of Bangladesh and belongs to the same genera as other more well-known species like cabbage, cauliflower
or broccoli. The whole plant is consumed in the cooked form in Bangladesh, but more often the swollen portion
of the plant below the ground is consumed. The leaves of Centella asiatica (L.) Urb. (Family: Apiaceae;
English: Asiatic pennywort; Bengali: thankuni) are also consumed in the cooked form as soup or as a vegetable
dish in Bangladesh, more so during episodes of gastrointestinal disorders like diarrhea, dysentery, bloating, and
indigestion. Occasionally, the plant is also consumed to increase memory. The fruits of Zizyphus mauritiana
Lam. (Family: Rhamnaceae; English: Indian plum; Bengali: boroi) are also consumed raw when ripe in
Bangladesh or taken in the form of pickles or chutney.
Diabetes is a disease affecting millions of people throughout the world and is manifested primarily by
increases in blood sugar levels, and in later stages can lead to complicated disorders like cardiovascular
problems, diabetic retinopathy and diabetic nephropathy. The disease has no known total cure in allopathic
medicine, but traditional medicinal practitioners of many countries, including Bangladesh, claim to have plant
remedies that can totally cure the disease. The leaves of the above three plants are often advised by the folk
medicinal practitioners of Bangladesh to be consumed in the form of decoction or in the form of cooked
vegetables for lowering of blood sugar in diabetic patients. According to projections made by the World Health
Organization, the number of diabetic patients in the world may increase by 35% within 2025 (Boyle et al.,
2001). As such, it is extremely important to find a total cure for diabetes before it reaches endemic proportions.
Various members of the Brassica oleracea family have been reported to have antihyperglycemic effects.
The antihyperglycemic and glycogenesis effects of cabbage (Brassica oleracea L. var. capitata) have been
reported in alloxan-induced diabetic rats (Asaduzzaman et al., 2011). Juice obtained from cabbage leaves is also
Corresponding Author: Dr. Mohammed Rahmatullah, Pro-Vice Chancellor and Dean, Faculty of Life Sciences University
of Development Alternative House No. 78, Road No. 11A (new) Dhanmondi, Dhaka-1205
Bangladesh
Tel: +88-01715032621; Fax: +88-02-815739; E-mail: [email protected]
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Dr. Mohammed Rahmatullah et al, 2013
Advances in Natural and Applied Sciences, 7(5) December 2013, Pages: 519-525
used as traditional medicine for treatment of diabetes by inhabitants of Douala Town, Cameroon (Din et al.,
2011). Aqueous extract of cabbage has also been shown to improve a number of parameters in diabetic rats
(Luka and Tijjani, 2013). The antidiabetic effect of Korean traditional Baechu (Chinese cabbage) kimchi has
been shown in type 2 diabetic rats (Islam and Choi, 2009). Amelioration of diabetic nephropathy by extract of
red cabbage has been reported (Kataya and Hamza, 2007).
The antidiabetic effect of ethanol extract of Centella asiatica leaves in alloxan diabetic rats has been
reported (Rahman et al., 2012). The plant juice has also been shown to exert antidiabetic activity in Type 1
model of alloxan induced diabetic rats (Rahman et al., 2011). In glucose tolerance tests, ethanolic and
methanolic extract of leaves normalized glucose levels in alloxan induced diabetic rats (Chauhan et al., 2010).
Anti-diabetic activity of ethanol extract of whole plant has been shown in streptozotocin-induced diabetic rats
(Gayathri et al., 2011). The hypoglycemic activity of Ziziphus mauritiana aqueous-ethanol seed extract in
alloxan-induced diabetic mice has been demonstrated (Bhatia and Mishra, 2010). Various solvent extracts of
fruits of the plant also reportedly showed antihyperglycemic activity in glucose overloaded hyperglycemic rats
(Jarald et al., 2009).
Studies conducted by our research group have centered on ethnomedicinal surveys (Rahmatullah et al.,
2009a-c; Rahmatullah et al., 2010a-g; Rahmatullah et al., 2011a,b; Rahmatullah et al., 2012a-d), followed by
screening of the plants obtained for antihyperglycemic, antinociceptive and cytotoxic activities (Anwar et al.,
2010; Jahan et al., 2010; Khan et al., 2010; Mannan et al., 2010; Rahman et al., 2010; Rahmatullah et al.,
2010h; Shoha et al., 2010; Ali et al., 2011; Barman et al., 2011; Hossan et al., 2011; Jahan et al., 2011; Rahman
et al., 2011; Sutradhar et al., 2011; Ahmed et al., 2012; Arefin et al., 2012; Haque et al., 2012; Sathi et al.,
2012). As part of the screening process to locate plants with antihyperglycemic properties, this study was
conducted to evaluate the antihyperglycemic potential of methanol extract of leaves of Brassica oleracea,
Centella asiatica, and Zizyphus mauritiana in oral glucose tolerance tests (OGTT) in glucose-overloaded mice.
MATERIALS AND METHODS
Leaves of Brassica oleracea were collected from Dhaka district, Bangladesh during January, 2013. The
plant was taxonomically identified at the Bangladesh National Herbarium at Dhaka (Accession Number 38,099).
The sliced and air-dried leaves of Brassica oleracea were grounded into a fine powder and 100g of the powder
was extracted with methanol (500 ml) for 48 hours. The extract was evaporated to dryness. The final weight of
the extract was 3g. Leaves of Centella asiatica were collected from Dhaka district, Bangladesh during May,
2013. The plant was taxonomically identified at the Bangladesh National Herbarium at Dhaka (Accession
Number 38,359). The sliced and air-dried leaves of Centella asiatica were grounded into a fine powder and 57g
of the powder was extracted with methanol (300 ml) for 48 hours. The extract was evaporated to dryness. The
final weight of the extract was 4.35g. Leaves of Zizyphus mauritiana were collected from Dhaka district,
Bangladesh during June, 2013. The plant was taxonomically identified at the Bangladesh National Herbarium at
Dhaka (Accession Number 38,560). The sliced and air-dried leaves of Ziziphus mauritiana were grounded into
a fine powder and 100g of the powder was extracted with methanol (500 ml) for 48 hours. The extract was
evaporated to dryness. The final weight of the extract was 5g.
Chemicals:
Glacial acetic acid was obtained from Sigma Chemicals, USA; aspirin, glibenclamide and glucose were
obtained from Square Pharmaceuticals Ltd., Bangladesh.
Animals:
In the present study, Swiss albino mice (male), which weighed between 15-22 g were used. The animals
were obtained from International Centre for Diarrheal Disease Research, Bangladesh (ICDDR,B). All animals
were kept under ambient temperature with 12h light followed by a 12h dark cycle. The animals were
acclimatized for three days prior to actual experiments. The study was conducted following approval by the
Institutional Animal Ethical Committee of University of Development Alternative, Dhaka, Bangladesh.
Antihyperglycemic activity:
Glucose tolerance property of the various extracts was determined as per the procedure previously
described by Joy and Kuttan (1999) with minor modifications. In brief, fasted mice were grouped into six
groups of six mice each for Brassica oleracea, six groups of five mice each for Centella asiatica, and six groups
of five mice each for Zizyphus mauritiana. The various groups received different treatments like Group 1
received vehicle (1% Tween 80 in water, 10 ml/kg body weight) and served as control, group 2 received
standard drug (glibenclamide, 10 mg/kg body weight). Groups 3-6 received methanol extract of leaves at doses
of 50, 100, 200 and 400 mg per kg body weight. Each mouse was weighed and doses adjusted accordingly prior
to administration of vehicle, standard drug, and test samples. All substances were orally administered.
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Advances in Natural and Applied Sciences, 7(5) December 2013, Pages: 519-525
Following a period of one hour, all mice were orally administered 2 g glucose/kg of body weight. Blood samples
were collected 120 minutes after the glucose administration through puncturing heart. Blood glucose levels were
measured by glucose oxidase method (Venkatesh et al., 2004).
Statistical analysis:
Experimental values are expressed as mean ± SEM. Independent Sample t-test was carried out for statistical
comparison. Statistical significance was considered to be indicated by a p value < 0.05 in all cases.
RESULTS AND DISCUSSION
At doses of 50, 100, 200 and 400 mg per kg body weight, administration of extract of Brassica oleracea
leaves led to reductions in blood glucose levels in glucose-loaded mice by, respectively, 22.4, 24.2, 34.0, and
47.6%. The results were both dose-dependent, as well as statistically significant. In comparison, a standard
antihyperglycemic effect, glibenclamide, when administered at a dose of 10 mg per kg body weight, reduced
blood glucose level by 41.3%. Thus at the highest dose of the Brassica oleracea extract tested (400 mg), the
extract demonstrated better antihyperglycemic potential than the standard drug, glibenclamide. The results are
shown in Table 1.
At the afore-mentioned four doses, i.e. 50, 100, 200 and 400 mg per kg body weight, administration of
extract of leaves of Centella asiatica led to dose-dependent and significant reductions in blood glucose levels in
mice by 29.4, 32.8, 33.6, and 35.7%, respectively. Glibenclamide, when administered at a dose of 10 mg per kg
body weight, reduced blood glucose level in this group of mice by 48.9%. The results are shown in Table 2. At
the same four doses, administration of extract of leaves of Zizyphus mauritiana lead to dose-dependent and
significant reductions in blood glucose levels by 37.8, 38.9, 40.5, and 43.1%, respectively. With this group of
mice, glibenclamide reduced the blood glucose level by 54.2%. The results are shown in Table 3. Notably, the
effect of glibenclamide varied somewhat from group experiment to group experiment, but nevertheless fell
within the range of 41.3 – 54.2%. This is not unusual, given that the weight of mice varied between the three
experiments conducted with the three different extracts. But overall it can be concluded that all extracts
demonstrated significant antihyperglycemic potential.
Several mechanisms can be attributed to the observed lowering of blood glucose by the extracts in the
present study. Glucose absorption in gut may be inhibited by a compound or compounds, as observed with
Mangifera indica L. (Anacardiaceae) stem-barks (Bhowmik et al., 2009). Another possible mechanism can
possibly be increase of peripheral glucose consumption induced by the extract, as has been seen with ethanolic
extract of Sapindus trifoliatus L. (Sapindaceae) (Sahoo et al., 2010). Alternately, antihyperglycemic compound
or compounds present in the extract may lower blood sugar either through potentiating the pancreatic secretion
of insulin or increasing the glucose uptake, as has been observed in studies with Artemisia extract and extract of
Ageratum conyzoides L. (Asteraceae), respectively (Farjou et al., 1987; Nyunai et al., 2009). The exact
mechanism for lowering of blood glucose by the three extracts has not been determined in the present study and
is currently ongoing in our laboratory.
Brassica oleracea var. gongylodes has been reported to contain quercetin (Duke, 1992). The anti-diabetic
effect of quercetin has been confirmed in rats (Abdelmoaty et al., 2010). Centella asiatica is known to contain a
number of bio-active compounds, including kaempferol and quercetin derivatives, brahmoside, brahminoside,
beta-sitosterol, and kaempferol (Duke, 1992). The hypoglycemic and antioxidant potential of kaempferol-3,7(O)-alpha-dirhamnoside has been shown (de Sousa et al., 2004). Beta-sitosterol also has been shown to have
anti-diabetic efficacy through lowering of blood glucose levels, which has been attributed to its ability to
increase peripheral glucose consumption (Karan et al., 2012). Brahmoside and brahminoside has been shown to
exert hypoglycemic effects in rats (Ramaswamy, 1970), which may also explain the observed antihyperglycemic
action of Centella asiatica leaf extract. Zizyphus mauritiana reportedly contains betulinic acid (Duke, 1992).
Betulinic acid has been shown to be a component of Morus alba root bark extract, which exerted a
hypoglycemic effect in streptozotocin-induced diabetic rats (Singab et al., 2005). Betulinic acid reportedly is
also an alpha-glucodidase inhibitor, which may explain its hypoglycemic action (Benalla et al., 2010). The
beneficial effect of pentacyclic triterpenoids like betulinic acid in diabetes and diabetes-induced complications
has been reviewed (Alqahtani et al., 2013).
Taken together, the results obtained in the present study suggest that consumption of Brassica oleracea and
Centella asiatica may prove beneficial to diabetic patients, when consumed on a regular basis. Studies are
ongoing in our laboratory for identification of the responsible phytochemicals in leaves of all three plants for the
observed antihyperglycemic effects, and the mechanisms through which the phytochemicals are exerting their
antihyperglycemic actions.
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Advances in Natural and Applied Sciences, 7(5) December 2013, Pages: 519-525
Table 1: Effect of methanol extract of Brassica oleracea leaves on blood glucose level in hyperglycemic mice following 120 minutes of
glucose loading.
Treatment
Dose (mg/kg body Blood glucose level (mmol/l)
% lowering of blood
glucose level
weight)
Control (Group 1)
10 ml
5.50 ± 0.31
Glibenclamide (Group 2)
10 mg
3.23 ± 0.14
41.3*
Brassica oleracea (Group 3)
50 mg
4.27 ± 0.43
22.4*
Brassica oleracea (Group 4)
100 mg
4.12 ± 0.32
24.2*
Brassica oleracea (Group 5)
200 mg
3.63 ± 0.35
34.0*
Brassica oleracea (Group 6)
400 mg
2.88 ± 0.28
47.6*
All administrations were made orally. Values represented as mean ± SEM, (n=6); *P < 0.05; significant compared to hyperglycemic control
animals.
Table 2: Effect of methanol extract of Centella asiatica leaves on blood glucose level in hyperglycemic mice following 120 minutes of
glucose loading.
Treatment
Dose (mg/kg body Blood glucose level (mmol/l)
% lowering of blood
weight)
glucose level
Control (Group 1)
10 ml
4.70 ± 0.38
Glibenclamide (Group 2)
10 mg
2.40 ± 0.21
48.9*
Centella asiatica (Group 3)
50 mg
3.32 ± 0.33
29.4*
Centella asiatica (Group 4)
100 mg
3.16 ± 0.26
32.8*
Centella asiatica (Group 5)
200 mg
3.12 ± 0.20
33.6*
Centella asiatica (Group 6)
400 mg
3.02 ± 0.33
35.7*
All administrations were made orally. Values represented as mean ± SEM, (n=5); *P < 0.05; significant compared to hyperglycemic
control animals.
Table 3: Effect of methanol extract of Zizyphus mauritiana leaves on blood glucose level in hyperglycemic mice following 120 minutes of
glucose loading.
Treatment
Dose (mg/kg body Blood glucose level (mmol/l)
% lowering of blood
weight)
glucose level
Control (Group 1)
10 ml
5.24 ± 0.37
Glibenclamide (Group 2)
10 mg
2.40 ± 0.21
54.2*
Zizyphus mauritiana (Group 3)
50 mg
3.26 ± 0.24
37.8*
Zizyphus mauritiana (Group 4)
100 mg
3.20 ± 0.29
38.9*
Zizyphus mauritiana (Group 5)
200 mg
3.12 ± 0.30
40.5*
Zizyphus mauritiana (Group 6)
400 mg
2.98 ± 0.18
43.1*
All administrations were made orally. Values represented as mean ± SEM, (n=5); *P < 0.05; significant compared to hyperglycemic
control animals.
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