Phenolic compounds of Senna alata extracts and
their Inhibitory activity of α-Glucosidase
Ousmane Ilboudo1, Têeda Hamidou Ganamé1,
Wende-konté Hazaël Conania Nikiéma1,
July Adelaïde Konané1, Yssouf Karanga1,2,
Issa Tapsoba1*
1Laboratoire
de Chimie Analytique, Environnementale et Bio-Organique (LCAEBiO),
Université Joseph KI-ZERBO, 03 BP 7021 Ouaga 03,
Ouagadougou, Burkina Faso.
2Laboratoire
de Chimie Analytique, Physique Spatiale et Energétique (LCAPSE),
Université Norbert ZONGO, Avce Maurice Yameogo, BP 376
Koudougou, Burkina Faso.
*Corresponding Author E-mail: issa.tapsoba@ujkz.bf
INTRODUCTION:
Diabetes mellitus is a chronic, non-communicable
disease that today represents a major public health problem worldwide1.
According to the World Health Organization (WHO), the global prevalence of
diabetes has increased significantly, affecting around 10% of the adult
population in 2021, or approximately 536.6million people, with projections
reaching 783.2million by 2045 according to international diabetes federation2.
Burkina Faso has not remained on the sidelines of this scourge. Indeed, in
2013, a national survey estimated diabetes prevalence at 4.9% nationwide among
people aged 25 to 64. This proportion has been rising steadily, reaching 7.6%
by 2021, with the prevalence of abnormal blood sugar levels (pre-diabetes)
estimated at 16.8%3. This pathology is characterized by chronic
hyperglycemia due to disturbances in insulin secretion and/or inaction3.
The complications associated with diabetes, notably cardiovascular disease,
nephropathy, neuropathy and retinopathy, considerably reduce the life expectancy
of patients4 making it a priority for researchers worldwide.
Different types of antidiabetic drugs are employed in the treatment of Diabetes
with several different mechanisms, as, suppressing hepatic glucose production
(biguanides)5; stimulating insulin secretion (sulfonylureas and
glinides)6; delaying digestion and absorption of carbohydrates to
maintain postprandial glucose levels (inhibitors of α-glucosidase and
α-amylase); increasing insulin receptor sensitivity; and glucose uptake in
peripheral tissues (thiazolidinedione and metformin) or insulin7. In
type 2 diabetes, the treatment with an α-glucosidase inhibitor is
beneficial in delaying postprandial glucose uptake. The enzyme
α-glucosidase contributes to the conversion of carbohydrates to glucose.
Glucose levels in the blood can be reduced back to normal by blocking the
enzyme α-glucosidase8,9.
In the context of current treatments as stated above,
although oral antidiabetics and insulin therapy are effective, the cost of
treatment is almost unbearable for certain social strata, reducing their
accessibility in certain regions of sub-Saharan Africa. In addition, they often
have undesirable side effects for patients10. An alternative is to
turn to medicinal plants, which are an inexhaustible and valuable source of
bioactive compounds11. Traditional medicine plays a crucial role in
the healthcare systems of developing countries12. In Africa, over
80% of the population use medicinal plants for their primary health needs and
for the management of certain diseases, such as diabetes13.
Indeed, the various parts of these plants contain
secondary metabolites such as phenolic compounds capable of regulating blood
sugar levels in diabetic patients. Several studies have established a
correlation between the antidiabetic properties of plant extracts and their
content of phenolic compounds, including flavonoids and tannins14. A
number of studies carried out in our laboratory on plants such as Euphorbia
hirta, Leptadenia hastata15,16, Cassia occidentalis17
and Acacia macrostachya18 have shown that extracts rich in
flavonoids and other phenolic compounds from these plants have notable
antidiabetic properties. Among Burkina Faso’s local medicinal plants, Senna
alata (L.) Roxb. a Fabaceae widely used in traditional medicine19,
is attracting growing interest due to its numerous biological and
pharmacological properties20. Preliminary studies on the plant have
documented potential antidiabetic properties linked to the presence of
bioactive secondary metabolites, such as flavonoids and anthraquinones21,22.
The present study investigated the antidiabetic effect of Senna alata,
focusing on α-glucosidase inhibition effect by different extracts of the
plant.
MATERIAL AND METHODS:
Leaves and flowers of Senna alata were
collected in October 2024 from Ouagadougou, capital of Burkina Faso, at GPS
coordinates N12°19'9.23" and W1°28'2.89". The specimens were
identified by a botanist from the laboratory of biology and vegetable ecology
at University of Joseph KI-ZERBO. After being carefully washed, the various
harvested organs were dried in a sunlight-free enclosure for two (02) weeks
under ventilation. The dried plant material was then ground to a fine powder
using an electric grinder and stored for further
processing.
Extraction Methods:
In this study, two extraction techniques were used: aqueous and
hydroalcoholic maceration (ethanol-water 70% v/v) and decoction. The principle
of this method is based on the difference in the affinity of phytoconstituents
between a solid phase (plant powder) and a liquid phase (solvent).
Maceration was carried out separately using two
different solvents: distilled water and a hydroalcoholic mixture (ethanol-water
70% v/v). 50g of dry powder were macerated in 400mL of solvent for 24h at room
temperature. After filtration on Wattman N°1 filter paper, the filtrates
obtained were concentrated using a rotary evaporator and then freeze-dried to
obtain the aqueous extracts (FeMAq) for leaves, (FlMAq) for flowers and
hydroalcoholic extracts (FeMHA) for leaves, (FlMHA) for flowers.
Decoction:
50g of dry plant material were introduced into a 1L Erlenmeyer flask
containing 400mL distilled water. The mixture was boiled for 30min. After
cooling, the mixture was filtered through Wattman N°1 filter paper. The
filtrates obtained were then concentrated using a rotary evaporator and
freeze-dried to give the decocted extracts noted (FeD) for the leaves and (FlD)
for the flowers.
Chemical screening:
Chemical screening is a qualitative characterization
designed to highlight the different secondary metabolites present in each plant
extract. This preliminary step is vital importance in the study of the
biological properties of a plant extract, as it enables biological tests to be
oriented according to the metabolites detected23. In this work, two
complementary analytical methods were used to identify the various secondary
metabolites contained in the extracts: qualitative tests with specific reagents
and thin-layer chromatography (TLC).
Determination of Total Phenolic Compounds:
The content of total phenolic compounds in the various
extracts was determined using the Folin-Ciocalteu method, based on a redox
reaction24. Phenolic compounds, via their hydroxyl (-OH) and
carboxyl (-C=O) groups, reduce phosphotungstic and phosphomolybdic acids to
blue phosphotungstate and phosphomolybdate complexes according to equation 1. The
procedure involves mixing 60µL of extract and 60 µL of Folin-Ciocalteu reagent
(FCR). The reaction mixture is incubated for 8 min, then 120µL of a 7.5% (w/v)
sodium carbonate solution (Na2CO3) are added. The whole
is incubated again for 1h at ambient laboratory temperature. Absorbances were
read at 760 nm using a UV-Visible spectrophotometer (SPECTROstar NANO). Total
phenolic compound content is obtained by plotting absorbance readings against a
previously established gallic acid calibration curve. Values are expressed in
micrograms of gallic acid equivalent per milligram of dry extract (µg EGA/mg
extract).
Equation 1.
Reduction of Mo6+or W6+ions to Mo5+ or W5+
by gallic acid
Determination of Total Flavonoids:
Total flavonoids were determined using the aluminum
trichloride colorimetric method described by Zhishen et al. in 199925
with some modifications. This method involves the complexation of flavonoids
via the hydroxyl groups (-OH) in the ortho position on rings A and B or the
keto (C=O) group C4 and the hydroxyl group C3 or C5 by
Al3+ ions derived from AlCl3 in a basic medium (equation
2). This complexation results in the formation of a pink complex whose
intensity is proportional to the flavonoid content of the extract. To achieve
this, 50µL of each suitably diluted sample are mixed with 150µL of distilled water,
followed by 15µL of 5% (w/v) sodium nitrite solution NaNO2. 5 min
later, 15µL of a 10% (w/v) AlCl3 solution is added. The mixture is
incubated at room temperature for 6 min. Add 50µL of NaOH (1N) and measure the
absorbance of the pinkish mixture at 510 nm using a UV-Visible
spectrophotometer (SPECTROstar NANO). A calibration curve was established
beforehand, using quercetin as a reference and following the same procedure.
The total flavonoids content of the sample, expressed in microgram quercetin
equivalent per milligram extract (µg EQ/mg extract), is obtained using the
equation for the quercetin calibration curve.
Equation 2.
Complexation of a flavonoid by Al3+ions in a basic medium.
Determination of condensed tannins:
Condensed tannins in the various extracts are
determined using the method described by Broadhurst and Jones26. In
acidic medium, the terminal units of condensed tannins react with vanillin to
form a red chromophore complex26 (equation 3). The intensity of the
coloration is proportional to the amount of condensed tannins initially present
in the sample27. To 400μL of the extract at different
concentrations, 3mL of vanillin solution (4% in methanol) and 1.5mL of concentrated
HCl are added. After 15minutes of reaction, the absorption is read at 500nm
using a SPECTROstar NANO UV-Visible spectrophotometer. Concentrations of
condensed tannins in extracts are deduced from the equation of the catechin
calibration curve (standard). Calculated values are expressed in microgram
catechin equivalent per milligram extract (µg EC/mg extract).
Equation 3.
Complexation of condensed tannin with vanillin in acid medium
Antioxidant Activity by DPPH Method:
The DPPH test measures the anti-free radical activity
of pure molecules or plant extracts. It measures the ability of an antioxidant
to reduce the DPPH● chemical radical
(2,2-diphenyl-1-picrylhydrazyl) by hydrogen transfer (equation 4). The DPPH●
radical, initially purple, is transformed into the pale-yellow DPPH-H. For this
experiment, 50µL of the extract are mixed with 200µL of DPPH●
radical. After 10 min incubation in the dark, the absorbance was read at 517 nm
using a SPECTROstar NANO UV-Visible spectrophotometer. The IC50 of
the various extracts, expressed in µg/mL, are determined by plotting half the
absorbance of the DPPH● radical without sample against the
regression curve of the samples.
Antidiabetic activity:
Antidiabetic activity was assessed by monitoring the
inhibitory effects of the different extracts on α-glucosidase enzyme
activity. As a reminder, α-glucosidase is a key enzyme for the hydrolysis
metabolism of oligosaccharides into absorbable monosaccharides (equation 5) in
the small intestine28,29. Its inhibition could therefore reduce
postprandial hyperglycemia30. The α-glucosidase inhibitory
activity of extracts was assessed according to the following protocol: a
mixture containing 20µL of the enzyme (1 Unit/mL), 120µL of phosphate buffer
(0.1M at pH 6.9) and 10µL of each extract at different concentrations was
introduced into 96-well microplates at 37°C. After 15 min pre-incubation, the
enzymatic reaction is initiated by adding 20µL of 5mM p-nitrophenyl-α-D
glucopyranoside (pNPG) solution prepared in 0.1M phosphate buffer (pH 6.9). The
reaction mixture is incubated for a further 15min at 37°C. The reaction is
stopped by adding 80µL of 0.2M sodium carbonate solution. Absorbance is read at
405nm using a SPECTRO star NANO UV-Visible spectrophotometer. The reaction
system without plant extracts is used as the control and the system without the
α-glucosidase enzyme is used as a blank to correct background absorbance.
Acarbose is the reference antidiabetic compound used. The inhibition rate of the α-glucosidase enzyme is
calculated using the following formula:
AC: Absorbance of control and AS: Absorbance of sample.
Equation 5. Hydrolysis reaction of
p-nitrophenyl-α-D glucopyranoside by the enzyme α-glucosidase to
glucose and para-nitrophenol
RESULTS AND DISCUSSION:
Extraction yields:
After extraction, the yields of the various
lyophilisates obtained were calculated as the ratio of the mass of the extract
to the mass of the plant powder. The results obtained are shown in Table 1.
Table 1. Yields of Senna alata leaf and flower
extracts
|
Extracts
|
Leaves
|
Flowers
|
|
Mass
(mg)
|
Yield
(%)
|
Mass
(mg)
|
Yield
(%)
|
|
Hydroalcoholic
|
11499.01
|
22.99
|
18634.30
|
33.77
|
|
Aqueous
|
10374.20
|
20.74
|
10567.30
|
21.13
|
|
Decocted
|
12454.80
|
24.90
|
16888.20
|
37.26
|
Analysis of the data in Table 1 reveals several
important trends depending on the solvent and temperature used for extraction.
Firstly, it is clearly seen, irrespective of the plant part used, decoction
gave the best extraction yields. This difference could be explained by the
effect of heat and the polarity of the solvents used. Indeed, the work of Okagu
and al. (2021)31 has shown that heat facilitates cell wall
disruption and the extraction of secondary metabolites. Furthermore, Obafemi
and al. (2017)32, Bohui and al. (2018)33 showed
in their works that decoction gave the best yields compare to maceration and
infusion. Furthermore, the data in the table show that Senna alata flowers
contain more secondary metabolites sensitive to the extraction methods used in
this study. This result corroborates the work of Yusuf and al. (2014),
who showed that flowers possess higher levels of polyphenols and other
secondary metabolites than other parts of the plant34. Finally, the
high extraction yield obtained is an added value in the valorization of
extracts from the plant species. Indeed, it has been shown that a high
extraction yield is a guarantee of efficiency in extracting a greater quantity
of bioactive compounds. These results show that the choice of solvent has a
significant influence on extraction yield, and that decoction is the most
efficient method for extracting secondary metabolites from Senna alata.
Total Phenolic Compound (TPC):
The phenolic compound content of the various Senna
alata leaf and flower extracts was determined using the gallic acid
calibration curve equation (figure 1a). Results are expressed in micrograms of
gallic acid equivalent per milligram of dry extract (μg EAG/mg) (figure
1b).
Figure 1b shows that Senna alata leaves and flowers are rich in phenolic
compounds, irrespective of the extraction technique used. Amongst the extracts,
the hydroalcoholic macerate (FeMHA) of the leaves showed the highest levels of
total phenolic compound, estimated at 284.06±2.69µg EGA/mg extract. On the
other hand, for both leaves and flowers, the decoctates (FeD and FlD) show the
lowest phenolic compound content. This could be to the consequence the thermal
degradation of certain thermolabile compounds. We can therefore confirm that
the levels of total phenolic compounds in Senna alata vary according to
the extraction solvent, technique and part of the plant used. Furthermore, the
high content of phenolic compounds in extracts, especially FeMHA, confers them
with numerous pharmacological properties, including antihyperglycemic
potential. Phenolic compounds have been shown to modulate key enzymes in
carbohydrate metabolism35.
Total flavonoid content (TFC):
Total flavonoid levels were determined using the
quercetin calibration curve equation (figure 2a). The results, expressed in
microgram quercetin equivalent per milligram dry extract (μg EQ/mg), are
shown in Figure 2b.
Figure 2. a) Quercetin calibration curve; b) Total flavonoid content of various Senna
alata extracts
Figure 2b reveals that all extracts contain
flavonoids, all parts combined. The highest contents are observed in the
hydroalcoholic extracts of leaves and flowers, with quercetin equivalents of
46.73±1.11μg and 35.83±1.08 μg respectively. These results are
consistent with data reported in the literature, which highlight the importance
of hydroalcoholic solvents for the extraction of flavonoids from Senna alata36.
Further analysis shows that hydroalcoholic and aqueous extracts of Senna
alata leaves have more TFC than those of flowers. However, we remark that
for the decoctated, flower extract FlD (27.90±2.35μg EQ/mg extract)
contains more TFC than leaf extract FeD (08.94±0.79μg EQ/mg extract). This
result could be explained by the presence of more heat-sensitive flavonoids in
the leaves than in the flowers. The presence of this subclass of phenolic
compounds in the extracts suggests that they could be good candidates in the
search for phytomedicines, especially antidiabetic ones.
Condensed tannins content (CTC):
The condensed tannins content of hydroalcoholic,
aqueous and decocted extracts of Senna alata leaves and flowers were
assessed using the vanillin method. The contents were determined from the
equation of the catechin calibration curve (figure 3a). The results, expressed
in microgram catechin equivalent per milligram dry extract (μg EC/mg), are
shown in figure 3b as histograms.
Figure 3b shows that Senna alata leaves and
flowers contain condensed tannins at levels ranging from 12.47± 0.35μg
EC/mg to 24.66±0.86μg EC/mg extract. On the other hand, the highest levels
were observed in aqueous extracts. These results, in line with data reported in
the literature [37], could be explained by the fact that condensed
tannins are more soluble in water than other organic solvents. We can therefore
conclude that the ideal method for extracting tannins from Senna alata leaves
and flowers is aqueous maceration.
The results of the chemical screening combined with
those of the phenolic, flavonoids and condensed tannins assay showed that the
leaves and flowers of Senna alata are rich in secondary metabolics of
various kinds. This great variability of phytoconstituents in extracts opens
prospectives for their use in a wide range of therapeutic applications,
including the management of oxidative stress and the treatment of diabetes. To
support this assertion, the antiradical and antihyperglycemic activities of
various extracts from the leaves and flowers of Senna alata were
evaluated.
The anti-free radical potential of each Senna alata
leaves and flowers extracts was measured by the DPPH
(2,2-diphenyl-1-picrylhydrazyl) assay, a widely used method for measuring the
ability of antioxidant compounds to neutralize free radicals. To this end,
calibration curves for the various extracts were drawn up, as shown in figure 4.
Figure
4. Calibration curves for various Senna alata
leaves and flowers extracts
The various equations in these curves were
used to calculate the 50% inhibitory concentration (IC50) of each
extract. All the results obtained are shown in Table 2.
Table 2. IC50 values (µg/mL) for different
extracts of Senna alata
|
Extracts
|
IC50
(µg/mL)
|
|
Leaves
|
Flowers
|
|
Hydroalcoholic
|
192.74 ± 0.41
|
326.20 ± 0.71
|
|
Aqueous
|
209.24 ± 0.59
|
328.33 ± 0.91
|
|
Decocted
|
335.43 ± 0.98
|
271.76 ± 0.69
|
|
Trolox
|
4.01 ± 0.01
|
Analysis of the results in this table shows that the
hydroalcoholic extract of Senna alata leaves is the most active, given
its low IC50 value (192.74μg/mL) compared with the other
extracts. This result corroborates those of the assay presented above, and
supports the hypothesis that the free radical scavenging activity of an extract
is correlated with the presence of phenolic compounds, flavonoids and condensed
tannins17. Comparative analysis also shows that Senna alata leaves
have better anti-free radical activity than flowers. These results are in line
with data reported in the literature38. In the remainder of our
study, therefore, only extracts from Senna alata leaves will be used to
assess antidiabetic activity.
The antidiabetic activity of Senna alata leaves
extracts was assessed by in vitro tests of α-glucosidase enzyme
inhibition. Inhibition of α-glucosidase is a one of the key therapeutic
strategy in the treatment of type 2 diabetes, as it slows down carbohydrate
digestion, thereby reducing the postprandial rise in blood glucose levels.
After evaluation, the inhibition percentages of the various Senna alata leaves
extracts and acarbose (reference) obtained are shown in figure 5.
Figure 5 shows that the percentage inhibition of
α-glucosidase enzyme activity is dose-dependent on extract or acarbose.
Moreover, we note that at a concentration of 0.368mg/mL the inhibition rate of
the three (03) Senna alata leaves extracts exceeds 90% while, acarbose
inhibits less than 70% even if at concentrations higher. It is clear from these
results that all Senna alata extracts appear to be more active than the
reference substrate. To support these results, the 50% inhibitory
concentrations (IC50) were calculated and the results reported in
Table 3.
Table 3. IC50 values for Senna alata leaf extracts
and acarbose
|
Extracts
|
IC50 (µg/mL)
|
|
Hydroalcoholic
|
52.01 ± 1.65
|
|
Aqueous
|
54.46 ± 1.04
|
|
Decocted
|
117.77 ± 8.02
|
|
Acarbose
|
280.73 ± 1.97
|
The results in Table 3 confirm the hypothesis raised
above that Senna alata leaf extracts are more active than acarbose,
regarding their lower IC50 values than the reference. It is common
to find that plant extracts have a more pronounced antidiabetic potential than
reference acarbose18,39,40. Furthermore, extracts containing the
highest levels of phenolic compounds (figure 1) and total flavonoids (figure 2)
showed the best antidiabetic activities. These results are in line with the
work of other authors41,42 who have shown that antidiabetic activity
correlates with phenolic and total flavonoid contents.
CONCLUSION:
The present work focused on the phytochemical study
and evaluation of the antidiabetic activity, relative to its α-glucosidase
enzyme inhibitory effect of extracts from Senna alata, a local plant
acclimatized in Burkina Faso and known for its various pharmacological
properties, particularly in the management of diabetics. The results obtained
show that Senna alata leaves and flowers contain number of chemical
groups, including phenolics, flavonoids and tannins in high concentrations,
especially in hydroalcoholic extracts. Investigation of the antihyperglycemic
potential revealed that the hydroalcoholic, aqueous and decocted extracts of Senna
alata leaves effectively inhibit the activity of the enzyme
α-glucosidase, compared with acarbose taken as a reference. Subject to
toxicity control, we can conclude that Senna alata leaf extracts are
good candidates for the formulation of antihyperglycemic phytomedicines.
CONFLICT OF INTEREST:
The authors have no conflicts of interest regarding
this investigation.
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