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In vivo inhibitory activities of husk extract and fractions of Zea mays on alpha amylase and alpha glucosidase | Advance Pharmaceutical Journal

Research Articles

2021  |  Vol: 6(6)  |  Issue: 6 (November-December) | https://doi.org/10.31024/apj.2021.6.6.2
In vivo inhibitory activities of husk extract and fractions of Zea mays on alpha amylase and alpha glucosidase

Jude E. Okokon1*, Godwin Enin2, Mandu E. Nyong1, Blessing C. Anyanwu2, Godswill F. Dick2

1Department of Pharmacology and Toxicology, Faculty of Pharmacy, University of Uyo, Uyo, Nigeria

2Department of Chemistry, Faculty of Science, University of Uyo, Uyo, Nigeria

*Address for Corresponding Author

Jude E. Okokon

Department of Pharmacology and Toxicology, Faculty of Pharmacy, University of Uyo, Uyo, Nigeria

 
 

Abstra​ct

Objective: Zea mays husk is used in Ibibio traditional medicine for the treatment of various ailments including diabetes mellitus, malaria and ulcer. Aim of present study was to investigate inhibitory activities of husk extract and fractions of Zea mays on alpha amylase and alpha glucosidase. Material and methods: The husk extract (187-561 mg/kg) and fractions (n-hexane, dichloromethane, ethyl acetate and methanol,374 mg/kg) of Zea mays were evaluated in rats for inhibitory effect on alpha amylase and alpha glucosidase enzymes using starch, sucrose and maltose as substrates. Acarbose was used as referenced drug. Results: The husk extract caused significant (p<0.05) reduction in blood glucose levels of treated rats though non dose-dependently with the various substrates used. The methanol fraction followed by ethyl acetate fraction exerted the highest inhibitory effect when starch and sucrose were used as substrates, while DCM fraction was the most active fraction when maltose was used as substrate. Conclusion: The results suggest that the husk and fractions of Z. Mays have the potentials to inhibit alpha amylase and glucosidase in rats.

Keywords: Zea mays, hypoglycaemia, alpha amylase, alpha glucosidase


Introduction

Zea mays L. (Poacae) commonly called maize or corn, is a grass and food plant cultivated for human and animal benefits. The plant is tall and bears ears that are enclosed in modified leaves known as husks (Simmonds, 1979). In addition to its nutritive values, various parts of the plants are used in ethnomedicine for the treatment of several ailments such as diabetes (Foster and Duke, 1990; Gill, 1992; Abo et al., 2008; Brobbey et al., 2017; Okokon et al., 2017a), cough (Gill, 1992), inflammatory diseases (Okokon et al., 2016), pains and arthritis (Owoyele et al., 2010) and ulcer (Jadhav, 2016). Reported pharmacological properties of the husk extract which include; analgesic, anti-inflammatory (Owoyele et al., 2010), antioxidant (Dong et al., 2014), antidepressant (Okokon et al., 2016), antimalarial and antiplasmodial (Okokon et al., 2017a), hepatoprotective (Okokon et al., 2017b; Okokon et al., 2020; Udobang et al., 2019), antidiabetic and hypolipidemic (Okokon and Mandu, 2018) and nephroprotective (Okokon et al., 2017c; Okokon et al., 2019), antiulcer (Okokon et al., 2018) and antiobesity (Okokon et al., 2021) activities. The median lethal dose (LD50) of the ethanol husk extract was determined to be 1874.83 mg/kg (Okokon et al., 2016).  Isolated compounds from the husk extract include; arabinoxylan (Ogawa et al., 2005), phenolic compounds (gallic acid, protocatechuic acid, chlorogenic acid, cafeic acid, femlic acid, rutin, resveratrol, and kaempferol) (Dong et al., 2014), anthocyannins (Li et al., 2008) and stigmasterol, stigmasteryl stearate and stigmasteryl palmitate (Okokon et al., 2021). In this study, we report in vivo alpha amylase and alpha glucosidase inhibitory activities of the husk extract and fractions of Zea mays.

Materials and methods

Collection of plant materials

Fresh husks of Zea mays were collected in August 2020 from Farmland in Uruan in Uruan LGA, Akwa Ibom State, Nigeria. The husks were identified and authenticated as Zea mays by a taxonomist in the Department of Botany and Ecological studies, University of Uyo, Uyo, Nigeria. Herbarium specimen (FPH, 614) was deposited at the Faculty of Pharmacy Herbarium, University of Uyo, Uyo.

Extraction

Fresh husk of Zea mays were washed, cut into smaller pieces and dried under shade for two weeks. The husks were further pulverized to powder using electric grinder. The powdered leaves material was divided into two parts; one part (1.5 kg) was macerated in 50% ethanol (7.5 L) for 72 hours at room temperature (28 ±2 40°C). While the other part, (1.5 kg) was successively and gradiently macerated for 72 h in each of these solvents (2 x 5L), n-hexane, dichloromethane, ethyl-acetate and methanol to give corresponding fractions of these solvents.  These were thereafter filtered, and the liquid filtrates were concentrated and evaporated to dryness in vacuo 400C using a rotary evaporator (BuchiLab, Switzerland). The yields of extract and fractions were calculated and they were stored in a refrigerator at -4°C, until used for the proposed experiments.

Animals

Swiss albino male rats (123 – 148g) used for these experiments were gotten from Animal house of Department of Pharmacology and Toxicology, University of Uyo. The animals were housed in standard cages and were maintained on a standard pelleted feed (Guinea feed) and water ad libitum. Permission and approval for animal studies were obtained from the College of Health Sciences Animal Ethics Committee, University of Uyo.

In vivo alpha-Amylase inhibitory study

Fifty Wistar rats were divided into 10 groups of 5 rats each. The rats in all groups were fasted for 18 h and fasting blood glucose concentration was first taken at 0 min before administration. Group I, as the normal control, received distilled water (10 mL/kg). Group II rats were orally administered starch at 2 g/kg body weight (orally with distilled water as vehicle) and distilled water (10 mL/kg) simultaneously. Rats in group III were administered starch (2 g/kg) and the standard drug (acarbose) at 100 mg/kg simultaneously. Groups IV,V and VI were administered simultaneously, starch (2 g/kg) and Zea mays extract at 187, 374 and 516 mg/kg respectively while groups VII-X rats were administered starch (2 g/kg) and fractions (n-hexane, dichloromethane, ethyl acetate and methanol)  at 374 mg/kg respectively. All administrations were done orally and blood glucose concentration was monitored at 30, 60, 90, 120 and 180 min (Gidado et al., 2019).

In vivo glucosidase inhibitory study

Similar procedure described above was employed for this study with sucrose and maltose used as substrates (Gidado et al., 2019).

Blood glucose determination

Drops of blood from tip of rats’ tails were dropped on stripes and glucose concentration was measured using a glucometer according to manufacturer’s specifications (Accu-chek, Indiana). The glucometer works with the following principle; the blood sample is exposed to a membrane covering the reagent pad (strip), which is coated with an enzyme (glucose oxidase, glucose dehydrogenase). The reaction causes a colour change and the intensity of this change is directly proportional to the amount of glucose in the blood sample. Light from an LED strikes the pad surface and is reflected to a photodiode, which measures the light intensity and converts it to electrical signals. An electrode sensor measures the current produced when the enzyme converts glucose to gluconic acid. The resulting current is directly proportional to the amount of glucose in the sample (WHO, 2011).

Statistical analysis and data evaluation

Data obtained from this work were analysed statistically using ANOVA (one –way) followed by a post test (Tukey-Kramer multiple comparison test). Differences between means were considered significant at 5% level of significance ie p≤ 0.05.

In vivo alpha amylase and glucosidase inhibition assay

Results

Administration of starch (2 g/kg) caused varying percentages of increase in blood glucose concentrations after 30 mins. The percentages were starch (63.18%), extract/fractions treated groups (1.19-29.71%) and acarbose-treated group (17.97%). These increases were reduced after 90 min with animals treated with the middle dose of the extract (374 mg/kg) and methanol fraction having 0%, ethyl acetate group (13.80%) and n-hexane group (17.87%) increase in BGL. These decreases were significant and sustained for 180 min in middle dose (374 mg/kg), methanol and ethyl acetate fractions-treated groups. However, co-administration of the starch with acarbose prominently inhibited the rise in the blood glucose concentrations (Table 1).

Administration of sucrose (2 g/kg) produced a 46.01% increase in blood glucose concentration 30 minutes post-administration of the sucrose in the control group and 33.05-87.83 % increases in blood glucose concentration of extract/fractions-treated groups. The blood glucose concentrations were significantly reduced in lower doses (170 and 374 mg/kg) and methanol-treated groups after 90 mins with the 170 mg/kg treated group having no increase in BGL post-administration of sucrose. However, lower doses (170 and 374 mg/kg) and methanol fraction had the highest sustained effects throughout the duration of the study (180 min) (Table 2).

There was 60.78% increase in blood glucose concentration 30 min following maltose administration in the control group. However, 6.97-80.94% increases in BGL were observed in the extract/fractions-treated groups. The crude extract 170-510 mg/kg) significantly reduced blood glucose level though in a dose-dependent fashion after 90 min with highest dose (510 mg/kg) having 0% and middle dose (374 mg/kg) 1.74%, while dichloromethane fraction-treated group was found produced the most significant reduction in BGL among the fractions treated groups with 0% increase in BGL after 90 min. The extract (374 and 510 mg/kg) and dichloromethane fraction produced significant sustained effect throughout the duration of the study (180 min) (Table 3).

Table 1.   Effect of ethanol husk extract and fractions of Zea mays on Blood Glucose level of rat after oral administration of starch load

Treatment

Dose (mg/kg)

                                Blood Glucose Level Mg/Dl In Min

0 min

30 min

60 min

90 min

120 min

180 min

Control normal saline

-

86.00±11.53

87.66±7.12(1.93)

87.66±7.62(1.93)

73.66±6.17

91.0±7.50(5.81)

80.00±6.02

Starch

 

73.33±8.25

119.66±5.45a (63.18)

115.66±1.33a (57.72)

104.66±2.60a (42.72)

95.66±3.75a (30.45)

92.0±6.35(25.46)

Acarbose

100

72.33±2.69

85.33±12.97(17.97)

80.33±7.21(11.06)

76.33±3.48(5.53)

74.0±1.00(2.30)

72.33±8.68(0)

Crude extract

187

75.00±3.97

90.33±5.37a (20.44)

86.00±5.90(14.66)

77.33±3.71(3.10)

80.00±6.65(6.66)

76.33±6.36(1.77)

374

88.00±6.08

103.33±3.18a (17.42)

82.0±5.68

81.66±3.38a

63.66±2.40

78.66±4.05

561

83.00±4.72

107.66±2.33a (29.71)

95.66±2.33(15.25)

78.66±5.36

72.0±3.78

73.0±4.58

n-hexane fraction

374

87.66±6.98

107.0±5.01a (22.81)

103.33±2.07a (17.87)

89.33±8.87a (1.90)

95.66±9.73(9.12)

85.66±7.21

Dichloromethane fraction

374

76.66±4.84

95.33±3.84a (24.35)

98.33±5.17(28.26)

88.0±4.00a (14.79)

85.33±3.48\(11.30)

82.66±5.33(7.82)

Ethyl acetate fraction

374

96.66±7.26`

107.0±4.16a (10.69)

110.0±5.19(13.80)

94.30±6.64()

92.33±8.25()

95.33±10.33()

Methanol fraction

374

111.0±4.61

112.33±9.52a (1.19)

98.66±13.29()

88.66±10.41()

102.0±2.64()

99.66±2.40()

Data is expressed as MEAN ± SEM, Significant at ap<0.05, when compared to control. (n=6). Values in parenthesis are percentage increase in blood glucose concentrations compared to 0 min in the same group. 

Table 2.   Effect of ethanol husk extract and fractions of Zea mays on Blood Glucose level of rat after oral administration of sucrose load

Treatment

Dose (mg/kg)

Blood Glucose Level Mg/Dl In Min

0 min

30 min

60 min

90 min

120 min

180 min

Control normal saline

-

100.00±4.25

88.33±1.85

92.33±4.25

90.33±2.33

89.0±4.35

87.33±3.84

Sucrose

2000

92.0±4.04

134.33±2.90b(46.01)

128.66±5.45a (39.84)

117.33±4.66a(27.53)

97.66±0.66(6.15)

104.16±2.48(13.21)

Acarbose

100

90.33±2.48

86.66±2.90

82.0±6.00

79.33±2.96

71.66±3.75

78.0±3.78

Crude extract

187

74.0±2.64

139.0±8.50(87.83)

72.66±6.96b

71.33±0.66

75.0±4.72(1.35)

69.0±3.05

374

72.0±3.78

119.0±10.01b(65.27)

76.66±7.21a (6.47)

60.33±4.63

64.0±4.50

59.0±0.57

561

63.66±3.18

101.66±15.33a (59.69)

82.0±1.52a (28.80)

82.0±9.64(28.80)

72.33±6.69(13.61)

67.66±6.17(6.28)

n-hexane fraction

374

88.66±10.08

118.33±9.85a (33.05)

90.33±12.17a (53.65)

67.66±9.77(28.76)

78.66±11.31(46.15)

62.33±8.66(29.61)

Dichloromethane fraction

374

67.66±9.87

105.66±5.92a (56.16)

86.66±10.99a(28.08)

86.33±1.85a (27.59)

88.33±2.02\(30.54)

89.0±1.00(31.54)

Ethyl acetate fraction

374

77.66±13.64

 

141.0±17.08a (81.56)

96.66±0.88(24.46)

82.33±7.88(6.01)

94.33±0.66(21.46)

95.33±8.00(22.75)

Methanol fraction

374

88.66±1.33

126.0±3.05a (42.11)

90.0±4.93a (1.51)

82.0±1.73

80.6±4.33

73.0±4.00

Data is expressed as MEAN ± SEM, Significant at ap<0.05, bp< 0.01, when compared to control. (n=6). Values in parenthesis are percentage increase in blood glucose concentrations compared to 0 min in the same group.

Table 3.   Effect of ethanol husk extract and fractions of Zea mays on Blood Glucose level of rat after oral administration of maltose load

Treatment

Dose (mg/kg)

Blood Glucose Level Mg/Dl In Min

0 min

30 min

60 min

90 min

120 min

180 min

Control normal saline

-

100.00±4.25

88.33±1.85

92.33±4.25(1.80)

90.33±2.33(3.62)

89.0±4.35(1.55)

87.33±3.84(3.98)

Maltose

2000

82.30±2.14

132.33±1.90b(60.78)

130.22±2.45(58.22)

120.66±3.22a(46.60)

115.0±2.46(39.73)

106.22±4.24(29.06)

Acarbose

100

85.34±1.36

88.22±1.10(3.37)

86.0±2.20(0.77)

85.33±2.15()

84.26±1.14()

82.28±2.26()

Crude extract

187

70.0±3.46

126.66±1.85b(80.94)

105.66±10.13b(50.94)

61.66±5.04a

72.0±3.78(2.85)

78.0±2.64(11.42)

374

76.66±7.75

120.0±6.42b(56.53)

78.0±12.00a(1.74)

65.33±6.38 a

60.33±13.92

75.0±7.63

561

95.66±3.71

102.33±12.01a(6.97)

84.0±9.07a

65.33±7.44a

71.0±7.57

72.33±7.57

n-hexane fraction

374

71.33±9.82

92.33±10.17b(29.44)

92.66±8.41a(29.90)

68.66±4.33 a

83.33±6.17(16.82)

83.0±9.60(16.36)

Dichloromethane fraction

374

80.66±4.84

102.66±32.60b(27.27)

80.66±2.96b

79.66±4.05a

83.66±0.88a(3.71)

80.66±2.60

Ethyl acetate fraction

374

76.0±5.13

 

112.66±0.33(48.23)

 

120.0±6.65(57.89)

81.0±8.73(6.57)

91.0±7.78(19.73)

80.0±2.08(5.26)

Methanol fraction

374

71.0±10.06

124.0±12.74b(74.64)

93.33±5.92a(31.45)

74.33±2.96(4.69)

72.0±9.84(1.40)

79.66±4.41(12.19)

Data is expressed as MEAN ± SEM, Significant at ap<0.05, bp< 0.01, when compared to control. (n=6). Values in parenthesis are percentage increases in blood glucose concentrations compared to 0 min in the same group.

Discussion

The husk extract is used traditionally by the Ibibios of Southern Nigeria in the treatment of various ailments such as fever, convulsion, malaria, body pains, diabetes, diarrhea, jaundice and hepatitis (Okokon et al., 2006). Preliminary reports showed that the husk extract possesses antidiabetic activity (Okokon et al., 2010). This work was designed to explore the possible antidiabetic mechanism of action of husk extract and fractions of Zea mays especially its inhibitory potentials on alpha amylase and alpha glucosidase enzymes.

The extract was found to non dose-dependently inhibit increases in blood glucose concentration following starch administration with the methanol and ethyl acetate fractions exerting the most inhibition. Complete digestion of dietary polysaccharides like starch is achieved by the combined action of α-amylases and α-glucosidase enzymes. The α-amylase enzyme digests α-bonds of the α-linked polysaccharides yielding disaccharides, like maltose, which are further reduced to monosaccharides by membrane bound α-glucosidase enzymes (Kalra, 2014; Alongi and Anese, 2018). Inhibitions of these enzymes delay the digestion of ingested carbohydrates thereby resulting in a small rise in blood glucose concentrations following carbohydrate meals as was observed in this study. As a target for managing Type 2 diabetes mellitus, many medicinal plants have been reported to possess α-amylase and α-glucosidase inhibitory potential (Ibrahim et al., 2014; Esimone et al., 2001).

Similarly, the husk extract and fractions significantly inhibited blood glucose rise when co-administered with maltose and sucrose with methanol and dichloromethane fractions exerting the highest inhibitions respectively. Acarbose, the standard drug used in this study significantly inhibited blood glucose rise when co-administered with starch, maltose and sucrose.

Alpha-amylase and α-glucosidase inhibitions by plants extracts have been reported severally (Ishnava and Metisariya, 2018; Shirwaikar et al., 2005). Phytochemicals implicated as anti-diabetic agents, do so possibly through α-amylase and glucosidase inhibition. The phytochemicals in question include flavonoids, saponins, tannins and terpenoids (Yoshikawa et al., 1998; Ortiz-Andrade et al., 2007; Ishnava and Metisariya, 2018). Phytochemicals screening of the husk extract revealed the presence of saponins, tannins, flavonoids, alkaloids and terpenes (Okokon et al., 2017). Polyphenolic compounds from plants are known to cause several effects on the biological systems which include enzymes inhibitions (Kalita et al., 2018; Funke and Melzig, 2005). The phenolic compounds are known to be strong metal ion chelators and protein precipitation agents forming insoluble complexes with proteins as well as acting as biological oxidants (Ishnava and Metisariya, 2018). Anthocyanins, a water-soluble flavonoids, have been found to be richly present in corn husk especially in polar fractions (n-butanol or methanol) of the husk (Li et al., 2008). It has been reported that anthocyanins exert inhibitory activities on alpha amylase and alpha glucosidase (Kalita et al., 2018; Berger et al., 2020; Chen et al., 2020). This may explain the high inhibitory potential of the methanol fraction as observed in this study. They are also known to exert antidiabetic activity by stimulating insulin secretion resulting in increased serum insulin levels and reduced BGL (Zhang et al., 2015). This suggests likely involvement of insulin activity in the observed effect as diabetic rats treated with the methanol fraction of the cornhusk have been reported to have elevated serum level of insulin (Okokon and Mandu, 2018). The presence of the polyphenolic compounds in the husk extract and fractions may suggest that their inhibitory potential on α-amylase and the membrane-bound intestinal α-glucosidase enzymes may be similar to the mechanism proposed generally for the polyphenolic compounds. Furthermore, the GCMS analysis of the dichloromethane fraction revealed the presence of phytosterols such as stigmasterol and sitosterol as reported by Okokon and Mandu, (2018). These compounds have been reported to increase serum insulin levels in diabetic rats (Nualkaew et al., 2015) as observed in dichloromethane husk fraction-treated diabetic rats (Okokon and Mandu, 2018). Stigmasterol and sitosterol have been reported to exert inhibitory effects on alpha amylase and alpha glucosidase (Kumar et al., 2013; Gosh et al., 2014). The presence of anthocyanin, stigmasterol and sitosterol in the husk extract and fractions may be responsible for the significant inhibitory activities observed in this study.

Conclusion

The results of this study suggest that Zea mays husk extract and fractions possess inhibitory activity on alpha amylase and alpha glucosidase enzymes and this maybe one of the modes of antidiabetic activity of the husk extract and fractions of Zea mays which can be attributed to the activities of its phytochemical constituents.   

Acknowledgements

The authors are grateful to Mr Nsikan Malachy of Pharmacology and Toxicology Department for providing technical assistance.

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