In vitro and In vivo Hypoglycemic Effect of Wild Edible Termite Mushrooms

doi:10.21203/rs.3.rs-1983840/v1

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In vitro and In vivo Hypoglycemic Effect of Wild Edible Termite Mushrooms

https://doi.org/10.21203/rs.3.rs-1983840/v1

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Objective

Diabetes mellitus is characterized by the increase in glucose levels in the blood and serum because of a change in carbohydrates, fat and protein metabolism. Termite mushrooms are consumed for high nutrition and traditional medicine. The methanol extract of the four termite mushrooms; Termitomyces albuminosus, T. eurhizus, T. robustus and T. striatus f. ochraceus was tested for inhibition of alpha-amylase by the starch-iodine method, and effect on blood glucose level and body weight in alloxan-induced diabetic mice.

Results

The secondary metabolites in the methanol extract of termite mushrooms were screened. Alkaloid, flavonoid, polyose, steroid, glycoside, terpenoid, fatty acid and emodin were found in all the termite mushrooms. The extract of T. straitus f. ochraceus has shown a strong inhibition against porcine pancreatic alpha-amylase by 61.4% at 200 µg/ml concentration. The extracts of all termite mushrooms at 500 mg/kg showed a significant reduction in the blood glucose level after 15 days of administration. Extract of termite mushrooms in two doses (250 and 500 mg/kg) intraperitoneally administered to the alloxan-induced diabetic mice indicated a significant enhancement in their body weight as compared to diabetic mice. Hence, termite mushrooms can be used as a substitute supplement for the management of diabetes mellitus.

alloxan

alpha-amylase

antidiabetic

diabetic

termite mushroom

Mushrooms are the intact key source of biologically active natural products that play an exemplary role in maintaining and improving the quality of human life through food security [1]. Despite the availability of different sources of secondary metabolites for the approaches to the discovery of therapeutics drugs, mushrooms remain one of the best reservoirs [1–3]. Termitomyces R. Heim. (termite mushroom) is an edible basidiomycetes mushroom belonging to the Lyophyllaceae. Termite mushrooms grow in association with termites and are dependent on the organic matter brought by them from their feeding on trees [4]. The fungus helps the termites to degrade the plant-derived material on which they live. Termitomyces species are highly esteemed and widely consumed for their high nutritional value [5]. They have medicinal properties and are regarded as good for the brain and memory. Some medicinal properties including antioxidant, anti-rheumatic, anti-inflammatory, anticonvulsive, diuretic, neuro-protective, relaxation, wound healing, hypoglycemic, anticancer, and antimicrobial have been studied in some termite mushrooms [6–9, 4].

Diabetes mellitus is an emerging global health problem and a metabolic disorder in the endocrine system characterized by a loss of glucose homeostasis [10–12]. Linking from indigenous knowledge and ethnopharmacology, termite mushrooms can provide a reliable and open approach to the development of pharmaceutical drugs more effectively [13–16]. The ethnomedicinal practice of termite mushrooms is an attempt to assess the antidiabetic potential due to their no side effect, apparent efficiency, and reasonably economical and enigmatic biological secretion. Hence, the objectives of this study were to elucidate qualitative screening of phytochemicals of selected termite mushrooms and the inhibitory activity of their extracts against alpha-amylase and alloxan-induced type-2 diabetes in mice. The exploration of the antidiabetic properties of termite mushrooms may be exceedingly domineering for the potential development of antidiabetic drugs that play a role in human welfare.

The fruiting bodies of four termite mushrooms were collected from Chitwan National Park, Nepal. They were identified based on their morpho-taxonomic characteristics concerning the relevant literature [17–19]. The voucher specimens of Termitomyces albuminosus (accession no. 2-2-1666), T. eurhizus (accession no. 2-2-1668), T. robustus (accession no. 2-2-1672) and T. striatus f. ochraceus (accession no. 2-2-1674) have been deposited in the Natural History Museum of the Tribhuvan University, Nepal. A qualitative phytochemical analysis of the crude extract of termite mushrooms was carried out by standard protocol [20]. The methanol extract of termite mushrooms was tested for the qualitative screening of secondary metabolites like alkaloid, volatile oil, flavonoid, steroid, saponin, tannin, emodin, polyurenoid, phenolic compound, amino acid, reducing sugar and anthocyanin.

In-vitro alpha-amylase inhibitory assay of the extract of termite mushrooms was carried out by the starch-iodine method developed by Fuwa [21] with a slight modification [22]. The microplate-based alpha-amylase assay was initiated by adding 40 µl each of different concentrations (40, 80, 120, 160 and 200 µg/ml) of extract and 40 µl of porcine pancreas α-amylase (20 mg/50 ml) in 0.1 M potassium phosphate buffer at pH 7.0. The microplate was covered with a lid to minimize the evaporative loss during incubation. After 30 minutes of incubation at 37°C, 20 µl of 0.1 N HCl was added to stop the enzymatic reaction, followed by the addition of 100 µl of iodine reagent (20 mg I₂ and 200 mg KI dissolved in 100 ml of 0.1 M potassium phosphate buffer). The absorbance was measured for the iodine-treated samples at 620 nm. Acarbose, a known commercial inhibitor of alpha-amylase was used as a positive control. The percentage inhibition of alpha-amylase by the extracts was calculated as inhibition percentage = [(absorbance blank – absorbance extracts)/absorbance extract] × 100. The concentration of the extracts of termite mushrooms required for 50% inhibition of porcine pancreatic alpha-amylase (IC₅₀) was determined from the corresponding dose-response curve of percentage inhibition versus inhibitor concentration.

Six to eight-week-old albino mice of either sex, weighing about 30–35 g, were selected for an experiment. They were kept in maintained environmental conditions of temperature (22 ± 2°C), humidity (60 ± 1%) and a 12-hour light/dark cycle [23]. They were fed with standard commercially available pellets and water. The experiment was conducted following the rules and regulations of the Animal Ethics Committee, Government of Nepal. Diabetes was experimentally induced in mice by injecting them intraperitoneally with alloxan at a dose of 200 mg/kg [24]. The alloxan-injected mice were kept under observation for 3 days. The mice with fasting blood glucose levels greater than 150 mg/dL measured by glucosuria using disaster strips were considered diabetic mice [25]. The mice were divided into five groups of five mice each. The mice of group I (normal mice) were administered with normal saline (5 ml/kg), group II (diabetic control) were alloxan injected, group III (diabetic positive control) were administered with glibenclamide (10 mg/kg), group IV (diabetic test) were administered with extract (250 mg/kg) and group V (diabetic test) were administered with extract (500 mg/kg) [23]. Blood glucose level was measured on the 1st, 5th, 10th and 15th day by taking a blood sample from a tail vein puncture under light ether anaesthesia. The body weight of mice was also measured during blood glucose estimation.

The results were presented as mean ± standard error of the mean (SEM). The data were statistically analyzed using Microsoft Excel. Analysis of variance (ANOVA) was performed to find out the statistical significance of the difference of means in different parameters among different species. Paired t-test was applied to determine the significance of the differences in the means in different parameters between standard drugs and extracts. Differences of p < 0.05 were considered statistically significant.

Wild edible termite mushrooms generally have biologically active secondary metabolites with antioxidative properties. The alkaloid, flavonoid, polyose, steroid, glycoside, terpenoid, fatty acid and emodin were found in all the tested Termitomyces species. However, volatile oil was found in Termitomyces eurhizus and T. robustus, and saponin and anthocyanin were found in T. albuminosus and T. straitus f. ochraceus (Table 1). Tannin, phenol, protein and reducing sugar were absent in all the termite mushrooms. The volatile oil was absent in T. albuminosus, and saponin and anthocyanin were absent in T. eurhizus and T. robustus.

Table 1

Phytochemical screening on methanol extract of termite mushrooms.
SN	Compounds	T. albuminosus	T. eurrhizus	T. robustus	T. straitus f. ochraceus
1	Volatile oil	-	+	+	-
2	Alkaloid
	a. Mayer's test	+	+	+	+
	b. Wagner's test	+	+	+	+
	c. Hager's test	+	+	+	+
3	Flavonoid
	a. Lead acetate	+	+	+	+
	b. NaOH test	-	+	+	+
	c. Shinado test	+	+	+	+
4	Polyoses	+	+	+	+
5	Steroid test	+	+	+	+
6	Glycoside test	+	+	+	+
7	Terpenoid test	+	+	+	+
8	Saponin test	+	-	-	+
9	Tannin/Phenols	-	-	-	-
10	Proteins/Amino acid
	a. Ninhydrin test	-	-	-	-
	b. Xanthoproteic test	-	-	-	-
11	Anthocyanin test	+	-	-	+
12	Fatty acid	+	+	+	+
13	Reducing test	-	-	-	-
14	Emodin test	+	+	+	+
Presence (+) and absence (-)

In-vitro alpha-amylase inhibitory assay of methanol extracts of termite mushrooms was determined using the porcine pancreatic alpha-amylase. The methanol extract of Termitomyces straitus f. ochraceus showed a strong inhibition against porcine pancreatic alpha-amylase by 61.4% at 200 µg/ml concentration. Similarly, the methanol extracts of T. eurhizus, T. robustus and T. albuminosus have inhibited the porcine pancreatic alpha-amylase by 52.70%, 51.59% and 50.97% respectively at their 200 µg/ml concentration. The percentage inhibition of porcine pancreatic alpha-amylase by acarbose was found as 81.68% at its 200 µg/ml concentration. However, the percentage inhibition of porcine pancreatic alpha-amylase by the methanol extracts of termite mushrooms and acarbose has decreased with lower in their concentrations (Table 2). The concentration of the extracts of termite mushrooms required for 50% inhibition of porcine pancreatic alpha-amylase (IC₅₀) was determined from the corresponding dose-response curve. The IC₅₀ value of T. straitus f. ochraceus, T. robustus, T. eurrhizus and T. albuminosus have 166.96 µg/ml, 197.13 µg/ml, 221.63 µg/ml and 230.85 µg/ml respectively. It was significantly different from the IC₅₀ of acarbose (87.01 µg/ml) (Table 2).

Table 2

Percentage inhibition of alpha-amylase by different concentrations of acarbose and methanol extract of termite mushrooms and their IC₅₀ values.
Sample	Concentration (µg/ml)	Inhibition percentage	IC₅₀ (µg/ml)
Acarbose	200	81.67*	87.01*
	160	75.95*
	120	57.15*
	80	40.07*
	40	27.09*
Termitomyces albuminosus	200	50.97	230.85
	160	41.42
	120	30.12
	80	19.98
	40	11.31
Termitomyces eurhizus	200	52.70	221.63
	160	40.56
	120	30.44
	80	19.75
	40	9.83
Termitomyces straitus f. ochraceus	200	61.40	166.96
	160	44.93
	120	37.82
	80	32.93
	40	22.04
Termitomyces robustus	200	51.59	197.13
	160	43.10
	120	38.94
	80	17.79
	40	6.81

The effect on blood glucose level in alloxan-induced mice after intraperitoneal administration of methanol extracts of termite mushrooms at different doses and glibenclamide (10 mg/kg) displayed a gradual reduction in blood glucose level in a time and dose-dependent manner (Table 3). A noticeable increase in fasting blood glucose level was measured in alloxan-induced diabetic mice as compared with the normal non-diabetic mice. According to a two-way ANOVA analysis, there was a significant difference among the diabetic mice and the group of mice treated with methanol extracts of termite mushrooms up to 10 days of administration as compared to control (glibenclamide treated) and normal mice. Analysis of the Tukey test showed that extracts of all termite mushrooms at 500 mg/kg showed a significant reduction in the blood glucose level compared to the control group at 15 days of administration. Therefore, a higher concentration of all tested termite mushrooms can reduce blood glucose levels to normal values as in the non-diabetic mice.

Table 3

Blood glucose level in alloxan-induced diabetic mice after prolonged administration of drugs and methanol extract of termite mushrooms.
Group of mice treated	Blood Glucose Level (Mean ± SEM)
Group of mice treated	Day 0	Day 5	Day 10	Day 15
Non-diabetic mice	106.00 ± 3.78**	106.80 ± 1.49**	108.60 ± 3.69**	114.20 ± 2.13*
Diabetic mice	353.20 ± 19.39	356.00 ± 23.37	362.40 ± 29.45	368.40 ± 28.49
Glibenclamide (10 mg/kg)	304.00 ± 34.54*	264.40 ± 32.73*	226.20 ± 32.67*	178.80 ± 31.81*
Termitomyces albuminosus (500 mg/kg)	329.60 ± 35.23	317.20 ± 35.07	301.60 ± 34.54	292.00 ± 33.79*
Termitomyces albuminosus (250 mg/kg)	357.00 ± 38.27	352.80 ± 38.59	345.60 ± 37.64	337.40 ± 35.84
Termitomyces eurhizus (500 mg/kg)	332.80 ± 27.77	328.20 ± 27.53	326.60 ± 27.50	312.40 ± 28.41*
Termitomyces eurhizus (250 mg/kg)	366.80 ± 26.23	362.20 ± 28.54	346.20 ± 29.44	330.80 ± 30.98
Termitomyces robustus (500 mg/kg)	307.60 ± 22.43	300.80 ± 17.79	281.20 ± 19.01	266.20 ± 19.32*
Termitomyces robustus (250 mg/kg)	336.80 ± 38.11	332.40 ± 39.49	329.40 ± 39.86	320.40 ± 39.05
Termitomyces straitus f. ochraceus (500 mg/kg)	330.80 ± 23.60	306.60 ± 20.47	272.40 ± 15.71	227.80 ± 19.90*
Termitomyces straitus f. ochraceus (250 mg/kg)	359.80 ± 38.91	352.40 ± 38.49	341.40 ± 38.10	332.60 ± 38.05

The body weight of all group mice was also determined. The body weight of mice in the normal non-diabetic group was significantly increased than in an alloxan-induced diabetic group. The body weights of diabetic mice treated with glibenclamide and methanol extract of termite mushrooms were significantly increased in the dose and time-dependent manner (Table 4). Extract of termite mushrooms in two doses (250 and 500 mg/kg) intraperitoneally administered to the alloxan-induced diabetic mice indicated a significant enhancement in their body weight as compared to diabetic mice.

Table 4

Body weight of alloxan-induced diabetic mice after prolonged administration of glibenclamide and methanol extract of termite mushrooms.
Group of mice treated	Body Weight (Mean ± SEM)
Group of mice treated	Day 0	Day 5	Day 10	Day 15
Non-diabetic mice	28.80 ± 0.41	32.80 ± 0.37*	37.90 ± 0.48*	42.1 ± 0.81*
Diabetic mice	27.20 ± 1.08	30.00 ± 2.53	31.1 ± 1.35	35.1 ± 1.03
Glibenclamide (10 mg/kg)	27.4 ± 0.85	35.90 ± 1.50*	40.20 ± 1.24*	44.8 ± 0.93*
Termitomyces albuminosus (500 mg/kg)	27.30 ± 0.97	31.50 ± 1.27*	35.00 ± 0.57*	38.20 ± 0.37*
Termitomyces albuminosus (250 mg/kg)	27.30 ± 0.86	31.80 ± 0.86*	35.20 ± 0.66*	37.40 ± 0.75*
Termitomyces eurhizus (500 mg/kg)	29.90 ± 1.27	31.40 ± 1.19*	34.80 ± 1.37*	37.80 ± 1.12*
Termitomyces eurhizus (250 mg/kg)	25.80 ± 0.78	29.60 ± 1.51	33.30 ± 1.35*	37.40 ± 1.02*
Termitomyces robustus (500 mg/kg)	31.30 ± 2.03	30.90 ± 0.97	36.20 ± 1.02*	38.30 ± 0.83*
Termitomyces robustus (250 mg/kg)	27.60 ± 0.75	31.60 ± 0.81*	34.80 ± 0.80	38.50 ± 0.68*
Termitomyces straitus f. ochraceus (500 mg/kg)	27.20 ± 1.10	32.90 ± 0.67*	36.00 ± 0.65*	38.10 ± 0.84*
Termitomyces straitus f. ochraceus (250 mg/kg)	26.30 ± 0.83	28.60 ± 0.67	33.70 ± 0.80	37.50 ± 0.52*

Wild edible termite mushrooms have been used by people for their food and nutrition. They have been reported in the literature along with several traditional values. In the current study, the phytochemical screening was confined to methanol extract of fruiting bodies of four termite mushrooms: Termitomyces albuminosus, T. eurhizus, T. robustus and T. straitus f. ochraceus. The result exhibited the presence of alkaloids, phenols, flavonoids, steroids, terpenoids, tannins, saponins and anthocyanin under only qualitative analysis like the previous findings [5, 15]. The presence of such secondary metabolites leads to the possible values in the traditional uses of termite mushrooms in diabetic medicines [26]. The increase in fasting blood glucose concentration is an important characteristic feature of diabetes mellitus [27]. To establish the scientific evidence for their utilization in the management of diabetes, methanol extract of these termite mushrooms has been used for in-vitro and in-vivo assays [7, 28]. The in-vitro antidiabetic assay was carried out by alpha-amylase inhibition assay. In the in-vitro assay, the extracts of termite mushrooms that inhibit alpha-amylase at their higher concentration were significantly different from acarbose at p < 0.05. This is because of the presence of alkaloid, flavonoid, terpenoid, glycoside, etc. (see Table 1) in fruiting bodies of termite mushrooms which enhance their abilities to inhibit the alpha-amylase enzyme that indicates their antidiabetic activity [29]. The hyperglycemia in diabetic patients is control by dropping the glucose released after consuming termite mushrooms as food supplements [30, 31]. Thus, inhibition of alpha-amylase enzyme involved the delaying of postprandial hyperglycemia. Alloxan induces the diabetes mellitus by the destruction of pancreatic beta cells. One of the mechanisms for beta cell destruction is the intracellular generation of free radicals [32]. Furthermore, termite mushrooms may prevent the destruction or regeneration of the already alloxan-destroyed beta cells of the pancreas because they have potent antioxidant activity [4]. In addition, the antioxidative components containing methanol extracts of all the termite mushrooms administered to alloxan-induced diabetic mice have reduced the blood glucose level significantly in the mice [7]. The weight loss of diabetic mice is due to a deficiency of insulin which leads to a reduction in the level of protein synthesis [33]. In this study, there is a reduction in the body weight of diabetic mice as compared to normal mice. However, after the administration of extract of termite mushrooms in diabetic mice, the body weight was normalized. The capability of termite mushrooms to defend against weight loss may be due to the bioactive compounds. The termite mushrooms contribute to the inhibition of alpha-amylase activity and play a significant role in the reduction of blood glucose level.

However, termite mushrooms have anti-diabetic activity we could not go for the isolation single molecule having anti-diabetic properties due to unavailability of facilities.

Ethical approval and consent to participant: This research has involved the animals that were approved by the Animal Ethics Committee, Government of Nepal. Consent to participant is not applicable.

Consent for publication: Not applicable.

Availability data and materials: All data generated or analysed during this study are included in this published article.

Competing interest: The authors declare that they have no competing interests.

Funding: The present work was supported by BioResource and BioEnvironmental Consultant Services Private Limited, Kirtiur-5, Paliphal, Kathmandu, Nepal.

Author’s contribution: AP did the laboratory work and wrote draft. MRP did the statistical analysis and wrote manuscript. HPA conceptualized the work. All authors read and approved the final manuscript.

Acknowledgements: The authors are grateful to BioResource and BioEnvironmental Consultant Services Private Limited, Kirtiur-5, Paliphal, Kathmandu, Nepal for the financial support. We are also thankful to the Department of Plant Resources, Kathmandu, Nepal for the laboratory facilities.

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In vitro and In vivo Hypoglycemic Effect of Wild Edible Termite Mushrooms

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