INTRODUCTION:

Diabetes is a chronic disease that develops when blood glucose levels rise because the body cannot produce enough insulin or use it effectively¹. According to the WHO (World Health Organization), diabetes is characterized by a state of permanent hyperglycemia with fasting blood glucose levels greater than or equal to 1.26 g/L (7 mmol/L) on two occasions and or greater than or equal to 2 g/L (11 mmol/L) at any time of the day².

Insufficient production of insulin, production of defective insulin, or the inability of cells to use insulin properly and efficiently leads to hyperglycemia and diabetes³. In sub-Saharan Africa, the prevalence is between 0.2% and 12%⁴ and in Burkina Faso, in 2013, it was 4.9% for the people which age is comprising between 25 to 64 years⁵. The precariousness of the conditions of care for diabetics as well as the socio-economic indigence in developing countries, particularly in Burkina Faso, are all obstacles to a normal blood sugar level, which is essential for the prevention of complications in diabetics⁶.

The population of Burkina Faso, essentially rural, does not benefit from satisfactory health coverage. This is due to the high cost of modern medicines, which are generally inaccessible to all social classes. Indeed, 80% of the population lives from agriculture and livestock, sectors that are still very unprofitable and underdeveloped. And according to a report by the Burkinabe Ministry of Health in 2015, 43.9% of the population of Burkina Faso, at national level lived below the poverty line⁵.Medicinal plants are very common in our daily lives⁷, hence their use for primary health care needs. Indeed, these plants contain secondary metabolites with various biological activities and their use could contribute to better management of people with diabetes. After a meal, postprandial hyperglycemia is most pronounced in patients with diabetes. Inhibiting glucose uptake in the intestines could reduce postprandial state. α-glucosidase is a key enzyme for the metabolism of oligosaccharides to absorbable monosaccharides in the small intestine⁸. Inhibition of this enzyme may delay the digestion of carbohydrates, decreasing glucose uptake and therefore reducing postprandial hyperglycaemia. The polyphenols are able not only to reduce oxidative stress but also to inhibit carbohydrate hydrolyzing enzymes and thus preventing hyperglycemia⁹. Several medicinal plants including C. occidentalis¹⁰ have been reported for their anti-diabetic action¹¹^,¹². According to previous work, C. occidentalis contains phenolic compounds, flavonoids, steroids^13,14. Other studies highlighted the contribution of these compounds to antidiabetic activity¹⁵ and their presence would inhibit α-glucosidase which is responsible for the hydrolysis of polysaccharides. We reported in the present work, the phytochemical and antidiabetic studies of C. occidentalis, a herbaceous plant acclimatized in Burkina Faso.

MATERIALS AND METHODS:

Reagents:

In this study, standards such as quercetin, catechin, gallic acid, acarbose, para-nitrophenyl α- D-glucopyranoside, α-glucosidase were used without further purification. They are all purchased from SIGMA Aldrich.

Plant material:

The leaves and stems of C. occidentalis were collected around Ouagadougou at its GPS coordinates 12^o19'12.80''N; 1^o26'17.85''W. Professor Amadé OUEDRAOGO, a botanist at Plant Biology and Ecology Laboratory of University Joseph KI-ZERBO, identified this plant and specimens are deposited in the herbarium of University Joseph KI-ZERBO with the identification numbers 18013 for Cassia occidentalis L. Dried plant material was pulverized and transformed into fine powder using an electric grinder. The extraction was done using a protocol previously described by Karanga and al.,(2017)¹⁶ with some modifications.

Phytochemical screening:

The chemical screening was carried out in order to identify the main chemical compounds contained in each extract. Thus, the aluminium chloride test for flavonoids, the iron (III) chloride test for tannins and the soda test for quinones were performed. TLC was also realized using standards we had in order to identify qualitatively the flavonoids present in the different fractions using the following elution system: ethyl acetate-glacial acetic acid-formic acid-water (10:1.1:1.1:2.6) (v/v).

Determination of total phenolic compounds:

Total phenolic content in the different fractions was determined using the Folin-Ciocalteu method¹⁷. To 60 µL of each sample at different concentrations were added 60 µL of RFC and 120 µL of 7.5% (w/v) Na₂CO₃ added 8 min later. The reaction mixture was incubated for 1 h and the absorbance was measured at 765 nm with a SPECTRO star NANO multi-plate reader, BMG LABTECH, Ortenberg, Germany. Total phenolic contents are expressed in microgram equivalent of gallic acid per milligram of extract (µg EGA/mg extract).

Determination of total flavonoids:

Total flavonoids content were estimated using Chang and al. (2002) method¹⁸ with slight modifications. Indeed, 50 µL of plant fractions at different concentrations were added to 150 µL of distilled water followed by 15 µL of 5% (w/v) NaNO₂ 5 min later, 15 µL of 10% (w/v) AlCl₃ was added and the whole was incubated at room temperature for 6 min. 50 µL of 1 N NaOH was added and absorbance were measured at 510 nm. A calibration curve for quercetin was established and used to deduce the flavonoid content, expressed in microgram equivalent of quercetin per milligram of extract (µg EQ/mg extract).

Determination of condensed tannins:

Condensation of polyphenolic compounds with vanillin in an acid medium constitute the principle of this method. It is specific to flavan-3-ols¹⁹. Condensed tannins content is performed for different extracts according to the method of Broadhurst and Jones²⁰ with some modifications. To 400 μL of each sample with suitable dilutions, 3 mL of vanillin solution (4% in methanol) and 1.5 mL of concentrated HCl are added. After 15 minutes of reaction, the absorbance is read at 500 nm. Condensed tannins contents are deduced from the catechin calibration curve and are expressed in microgram equivalent of catechin per milligram of extract (µg EC/mg extract).

FRAP method:

FRAP assay was performed to investigate the reducing power. Piljac- Zegarac and al. 2009 method²¹ is used with slight modifications. To each 50 µL of the extract at different concentrations 200 µL of FRAP reagent is added. After 10 min incubation at laboratory temperature, the absorbance was measured of the intense blue stain is read at 595 nm. This optical density is plotted against the calibration curve established using trolox. The results are expressed in micrograms equivalent of trolox per milligram of extract (µg ET/mg extract).

DPPH method:

The radical scavenging activity was determined by using 2,2-diphenyl-1-picrylhydrazyl radical. Sanchez-Moreno (2002) method²² was used with slight modifications. Thus, 50 µL of the extract is added to 200 µL of DPPH solution. After 10 min of incubation, the absorbance was measured at 515 nm with a spectrophotometer. Radical scavenging activity was expressed as IC₅₀ in µg/mL.

Assay for α-glucosidase inhibitory activity:

Inhibition of fractions on α-glucosidase activity evaluated using Ranilla and al. (2010) method²³ with slight modifications. Thus, in a mixture containing 20 µL of α-glucosidase (1 unit/mL) and 120 µL of 0.1 M phosphate buffer pH 6.9, 10 µL of each plant fraction at different concentrations is introduced. Each solution obtained is pre-incubated in 96-well microplates at 37°C for 15 min. After incubation, enzymatic reaction is initiated by adding 20 µL of 5 mM p-nitrophenyl-α-D-glucopyranoside solution in 0.1 M phosphate buffer (pH 6.9) and the reaction mixture is incubated for a further 15 min at 37°C. The reaction is stopped by adding 80 µL of 0.2 M sodium carbonate solution. The absorbance is read at 405 nm by a spectrophotometer of the type SPECTROstar NANO, BMG LABTECH, Ortenberg, Germany. The reaction system without plant extracts is used as a control and the system without α-glucosidase is used as a blank to correct the background absorbance. Acarbose is used as a positive control.

The inhibition rate of α-glucosidase is calculated by the following formula:

Ac- As

% of inhibition = --------------- x 100

Ac: Absorbance of the control

As: Absorbance of the sample

RESULTS AND DISCUSSION:

Chemical screening

The phytochemical screening revealed that C. occidentalis contain tannins, quinones and flavonoids (Table 1).

Table 1: Results of the phytochemical screening

Chemical groups	C. occidentalis
	Leaves			Stems
	ACF	BUF	H2OF	ACT	BUT	H2OT
Flavonoids	+	+	+	+	+	+
Tannins	+	+	+	+	+	+
Quinones	+	+	+	+	+	+

The thin layer chromatography (TLC) performed confirmed the presence of flavonoids in the different fractions of C. occidentalis after spraying with Neu's reagent (fig. 1).

On the TLC plates, several spots of different colouring appear. The frontal references of each spot were calculated and recorded in Table 2. The analysis of Table 2 indicates the presence of quercetin in the ethyl acetate fractions of the leaves and stems of C. occidentalis at the head reference of 0.94.

Figure 1: TLC of different fractions of C. occidentalis, A: apigenin standard, Q: quercetin standard, R: rutin standard; For C. occidentalis leaves (1: ACF, 2: BUF, 3: H₂OF) and stems (1: ACT, 2: BUT, 3: H₂OT)

Table 2: Frontal references for C. occidentalis fractions, apigenin, quercetin and rutin

	*C. occidentalis* (Stems)		*C. occidentalis* (Leaves)
Standard and Fractions	Frontal references	Spotlight colours	Frontal references	Spotlight colours
Apigenin	0.94	Green	0.94	Green
Quercetin	0.94	Yellow	0.94	Yellow
Rutin	0.38	Red	0.38	Red
AcOET (ACT and ACF)	0.51	Pink-beige	0.18
	0.59	Light green	0.24	Green
	0.85	Light blue	0.48	Pink-beige
	0.94	Yellow	0.57	Light green
			0.84	Blue
			0.94	Yellow
BuOH (BUT and BUF)	0.21		0.18	Light green
	0.24	Light green	0.24	Light green
	0.51	Beige pink	0.48	Pink-beige
	0.59	Light green	0.57	Light green
	0.70	Light blue
H₂O (H₂OT and H₂OF)	0.21	Light blue	0.18
	0.26	Light blue	0.24
	0.50	Yellow	0.48	Blue

Figure 2: Histograms of total phenolic content of C. occidentalis. Figure 3: Histograms of total flavonoid content of C. occidentalis fractions

Phenolic compound content:

The results obtained from the evaluation of the total phenolic compound (TPC) content of the extracts of the plants studied are presented in the figure 2.

Figure 2 shows that ethyl acetate fractions of stems (ACT) and leaves (ACF) of C. occidentalis contain the highest contents of phenolic compounds, 821.8 and 528.9 μg EGA/mg respectively. For butanol fractions, the obtained values are ca. 513.1 and 484.3 μg EGA/mg extract for stems and leaves respectively. The lowest contents were obtained with the residual fractions H₂OF, H₂OT with values close to 61.2 and 32.8 μg EGA/mg of extract for leaves and stems respectively. These results could be explained by the fact that C. occidentalis contains compounds with medium polarity that have a high affinity with ethyl acetate. These results are in agreement with the literature data¹⁶.

Total flavonoid content:

As for the evaluation of the total flavonoid content (TFC) of the plants studied, the results obtained from the tests are represented in the following figure 3.

From these histograms, it can be seen that ethyl acetate fractions of C. occidentalis also contain high levels of total flavonoids estimated at 310.9 and 896.5 μg EQ/mg extract respectively for ACF and ACT. Butanol fractions of stems (BuT) and leaves (BuF) fractions have 187 and 124.9 μg EQ/mg extract respectively and the low levels obtained by the residual fractions (H₂OT= 13.1 μg EQ/mg of extract and H₂OF= 20.9 μg EQ/mg of extract). The higher contents obtained in the polar fractions of C. occidentalis could be explained by the presence of aglycones and glycosylated flavonoids in these fractions. These results are also in agreement with the work of Karanga and al. (2017)¹⁶.

Condensed tannin content:

The results for condensed tannins content (CTC) are presented below.

Figure 4: Histograms of condensed tannin content of C. occidentalis.

ACF, ACT fractions of C. occidentalis contain more condensed tannins than the other fractions (fig. 4). The contents are estimated at 631.9 and 122.8 µg EC/mg extract respectively, followed by BuT (63.6 µg EC/mg of extract) and BuF (40 µg EC/mg of extract) fractions. A comparative analysis shows that the leaves of C. occidentalis contain more condensed tannins than the stems.

Antioxidant activity:

FRAP and DPPH methods:

Figure 5 represents the results obtained from the evaluation of the antioxidant activities (FRAP and DPPH) of C. occidentalis extract.

Figure 5: Antioxidants content of C. occidentalis fractions using DPPH and FRAP methods.

The results obtained show that different fractions have antioxidant activities independently of the method used. In the case of C. occidentalis leaves, it was found that ACF had the highest antioxidant content followed by BuF with 82.96 and 47.93 µg ET/mg of extract respectively using DPPH method. This result is confirmed by those obtained by FRAP method (128.49 and 68.78 µg ET/mg of extract for ACF and BuF respectively) and could be explained by the fact that these fractions have the best amount of TPC and TFC contents. The same result is obtained for C. occidentalis stems, where ACT also has the highest antioxidant content, followed by BuOH at 114.06 and 77.72 µg ET/mg of extract respectively according to the DPPH method. The same trends are observed when antioxidant levels are assessed by the FRAP method ie. 167.06 and 75.79 µg ET/mg of extract for ACT and BuT respectively. These results could be explained by the high amount of TPC and TFC in these fractions²⁴^,²⁵. The high antioxidant activity is observed with fractions containing the high amounts of phenolic compounds and total flavonoids such as ACT and ACF of C. occidentalis. These results are in agreement with Quezada and al. (2004)²⁶, and Zhang and al. (2010)²⁷ who found similar results. Oxidative stress leads to cause of several disease as diabetes²⁸. Antioxidants work against damage caused by oxidative stress²⁹ and are believed to reduce the risk of developing type 2 diabetes and have benefits in reducing insulin resistance and protecting the vascular endothelium²⁸. Thus, the use of antioxidants properties of this plant by diabetic people could prevent long-term complications that may arise from diabetes³⁰.

α-Glucosidase inhibitory activity

Figure 6 presents the different results obtained on α-glucosidase inhibition.

Figure 6: Inhibitory activity of C. occidentalis stem (ACT, BUT and H₂OT) and leaves (ACF, BUF and H₂OF) fractions and acarbose on α-glucosidase

As illustrated on figure 6, one can see that α-glucosidase inhibition depends on concentration effect of plant fraction. For example, the percentage inhibition of α-glucosidase starts at 34.14% for 0.147 mg/mL and reaches 100% at 1.412 mg/mL of the ACT. These results show that the different fractions studied demonstrated the antidiabetic properties of C. occidentalis. For this activity, ACF and ACT fractions of C. Occidentalis showed their potential to inhibit α-glucosidase. Based on its IC_50,(table 3) close to 0.274 ± 0.003 mg/mL, ethyl acetate fractions of stems (ACT) is also active as the standard acarbose with an IC₅₀ ca. 0.215 ± 0.004 mg/mL. The obtained results show also that the ACF is also active with an IC₅₀ of 0.538 ± 0.011 mg/mL. These fractions have high levels of flavonoids. Many flavonoids from plants have been used in treatment of diabetes³¹. Their presence in these fractions could explain this activity³¹.

A deep analysis of these results shows a perfect correlation between the amount of total polyphenol compounds and antidiabetic properties and these results are in agreement with the data in the literature^32,33 .

Table3: IC₅₀values of different fractions and acarbose.

Plant	Fractions	IC₅₀ (mg/mL)
C. Occidentalis leaves	ACF	0.538 ± 0.011
	BuF	1.069 ± 0.009
	H₂OF	1.703 ± 0.018
C. Occidentalis stems	ACT	0.274 ± 0.003
	BuT	1.048 ± 0.012
	H₂OT	2.163 ± 0.006
Standard	Acarbose	0.215 ± 0.004

Relationship between the α‑glucosidase inhibition and total phenolic content and total flavonoid content:

According to the literature, flavonoids compounds demonstrated their potential inhibitory effects on the activity of α-glucosidase^32,34. Based on below results, one can speculated that the antidiabetic properties could be due to the presence of flavonoids derivatives and this can be justified by the value of correlation coefficients (R²) between phenolic compound amount, total flavonoids and α-glucosidase inhibition (figure 7).

Figure 7: Correlation between total phenolic content and total flavonoid content and α-glucosidase inhibition in the different fractions of C. occidentalis.

Indeed, these obtained results demonstrated that TPC of C. occidentalis, contribute more than 98% to the antidiabetic activity and more than 93% are due to TFC. These results are in agreement with literature^33,34 which established a link between the antidiabetic properties of plant extracts with their content of phenolic compounds particular flavonoids amount.

The obtained results demonstrate that ethyl acetate fractions of C. occidentalis could be used in the treatment of diabetic people.

CONCLUSION:

The objective of this work was to study the chemical composition and to evaluate the anti-diabetic potential of C. occidentalis fractions by monitoring their inhibitory effect on α-glucosidase and the antioxidant properties of these fractions. Our results show that the different fractions of C. occidentalis contain flavonoids, tannins and quinones. Among these flavonoids, TLC analysis revealed the presence of quercetin in the ethyl acetate fraction of C. occidentalis leaves and stems. The assay of the different family groups showed that stems and leaves had the highest content of phenolic compounds with 821.8 and 528.9 μg EGA/mg respectively. These same fractions showed the best contents of total flavonoids, which are estimated at 310.9 and 896.5 μg EQ/mg of extract respectively. The ethyl acetate fractions of C. occidentalis stems and leaves showed significant anti-diabetic properties with IC₅₀ values of about 0.274 ± 0.003 and 0.538 ± 0.011 mg/mL respectively compared to the reference acarbose with IC₅₀ of about 0.215 ± 0.004 mg/mL. The same fractions showed the highest FRAP values close to 167.055 ± 0.008 and 128.490 ± 5.227 μg TE/mg respectively and DPPH values of 114.062 ± 2.698 and 82.962 ± 3.189 μg TE/mg. These results establish a good correlation between anti-diabetic activity and the content of polyphenolic compounds and flavonoids present in each fraction. The implementation of bio-guided fractionations will allow us to characterize the bioactive molecules responsible for this activity.

ABBREVIATIONS:

AcOEt: ethyl acetate fraction

ACF: ethyl acetate fraction of C. occidentalis/ leaves

ACT: ethyl acetate fraction of C. occidentalis/stems

BuOH: n-butanol fraction

BuT: n-butanol fraction of C. occidentalis/ stems

BuF: n-butanol fraction of C. occidentalis/leaves

H₂O: residual aqueous

H₂OT: residual aqueous fraction of C. occidentalis/ stems

H₂OF: residual aqueous fraction of C. occidentals/ leaves

IC₅₀: 50% inhibitory concentration

CONFLICT OF INTEREST:

The authors declared that they have no competing interests.

ACKNOWLEDGMENTS:

We would like to acknowledge International Science Programme (ISP) through the African Network of Electroanalytical Chemists (ANEC) for their financial support.

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Received on 29.01.2023 Modified on 13.03.2023

Asian J. Research Chem. 2023; 16(4):257-264.

DOI: 10.52711/0974-4150.2023.00043