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The effects of hot air-dried white button mushroom powder on glycemic indices, lipid profile, inflammatory biomarkers and total antioxidant capacity in patients with type-2 diabetes mellitus: A randomized controlled trial
Hadiseh Hashemi Yusefabad1, Seyed Ahmad Hosseini2, Mehrnoosh Zakerkish3, Bahman Cheraghian4, Meysam Alipour5
1 Department of Nutrition, Faculty of Paramedicine, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran
2 Nutrition and Metabolic Diseases Research Center, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran
3 Health Research Institute, Diabetes Research Center, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran
4 Department of Epidemiology and Biostatistics, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran
5 Department of Nutrition, Shoushtar Faculty of Medical Sciences, Shoushtar, Iran
| Date of Submission | 18-May-2020 |
| Date of Decision | 05-Sep-2020 |
| Date of Acceptance | 02-Feb-2022 |
| Date of Web Publication | 29-Jul-2022 |
Correspondence Address:
Dr. Seyed Ahmad Hosseini
Nutrition and Metabolic Diseases Research Center, Ahvaz Jundishapur University of Medical Sciences, P.O. Box: 159613-5715794, Ahvaz
Iran
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/jrms.JRMS_513_20
Background: The inflammatory and metabolic responses to mushroom in type 2 diabetes mellitus (T2DM) are unknown. The study aimed to evaluate the effect of Hot Air-dried White Button Mushroom (HAD-WBM) powder on glycemic status, lipid profile, inflammatory markers, and total antioxidant capacity (TAC) in T2DM patients. Materials and Methods: This randomized controlled trial was conducted at Golestan Hospital, Ahvaz, Iran. Eligible patients were adults aged 20–50 with Type 2 diabetes. Patients were assigned to each group using a randomized block design with block randomization (n = 22, in each group). Randomization was performed by an assistant and group allocation was blinded for the investigator and participants. The intervention and control groups received 16 g/day HAD-WBM or cornstarch powder for 8 weeks. The primary outcomes of interest were fructosamine, fasting blood sugar (FBS), insulin, homeostatic model assessment for insulin resistance, and secondary outcomes were triglyceride, low-density lipoprotein (LDL), high-density lipoprotein, very-LDL, cholesterol, high-sensitivity C-reactive protein (hs-CRP), interleukin 6 (IL-6), and TAC. Results: After 8 weeks, a significant decrease was observed in fructosamine (−0.228 ± 0.36 vs. 0.03 ± 0.38; P = 0.02) and LDL (−13.05 ± 20.67 vs. 0.81 ± 21.79; P = 0.04) in the HAD-WBM group compared to the control group. No significant changes were observed in fasting insulin and FBS between the two groups. However, a significant within-group reduction (−28.00 ± 42.46; P = 0.006) was observed for FBS in the HAD-WBM group. In the HAD-WBM group, insulin resistance reduced significantly at the end of the study (From 4.92 to 3.81; P = 0.016), but it was not significantly different between the two groups. There was no significant difference in TAC, hs-CRP, and IL-6 between the two groups. Conclusion: Considering the results of this study about the beneficial effects of HAD-WBM on the improvement of glycemic indices and LDL in T2DM patients, it is recommended that HAD-WBM could be used to control T2DM.
Keywords: Diabetes mellitus, glucose intolerance, inflammation, Mushroom, randomized control trial, supplementation
How to cite this article:
Hashemi Yusefabad H, Hosseini SA, Zakerkish M, Cheraghian B, Alipour M. The effects of hot air-dried white button mushroom powder on glycemic indices, lipid profile, inflammatory biomarkers and total antioxidant capacity in patients with type-2 diabetes mellitus: A randomized controlled trial. J Res Med Sci 2022;27:49 |
How to cite this URL:
Hashemi Yusefabad H, Hosseini SA, Zakerkish M, Cheraghian B, Alipour M. The effects of hot air-dried white button mushroom powder on glycemic indices, lipid profile, inflammatory biomarkers and total antioxidant capacity in patients with type-2 diabetes mellitus: A randomized controlled trial. J Res Med Sci [serial online] 2022 [cited 2023 Mar 28];27:49. Available from: https://www.jmsjournal.net/text.asp?2022/27/1/49/352943 |
| Introduction | |  |
Diabetes mellitus (DM) is one of the most common metabolic disorders characterized by chronic hyperglycemia with impaired metabolism of carbohydrates, fat, and protein.[1] DM is associated with several microvascular and macrovascular complications such as retinopathy, nephropathy, neuropathy, cardiovascular diseases, hemorrhagic stroke, cognitive dysfunction, and depression.[2],[3],[4]
The International Diabetes Federation has predicted that by 2040, the number of people with diabetes worldwide will reach 642 million.[5] As the number of diabetic patients increases, failures in the treatment and the side effects of drugs caused patients to tend to use medicinal plants to treat type 2 diabetes mellitus (T2DM).[6] Studies showed that many medicinal plants can have beneficial effects on patients with T2DM.[7]
In the past several centuries, mushrooms in addition to being used as a source of food, have also been considered as potentially hypoglycemic and anti-diabetic agents due to their therapeutic properties.[8] Agaricus bisporus (WBM; white button mushroom), belongs to the family of basidiomycetes, is one of the most proliferating species of edible mushrooms throughout the world due to its unique biologically active compound and pharmaceutical properties.[9] WBM is a rich source of dietary fiber (chitin), essential and semi-essential amino acids, linoleic and linolenic acid, sterols, phenolic and indole compounds, vitamins, ergothioneine, copper, zinc, and selenium which have antioxidant, anti-inflammatory, anti-carcinogenic, and immune regulatory properties.[10],[11] Therefore, these confirm the nutraceutical and therapeutic properties of WBM.[11] Vitamin D (VD) plays a role in the pathogenesis of T2DM, through its direct effect on insulin secretion, pancreatic β-cell function, and action.[12] VD should be supplied through dietary sources. The fruit bodies of mushrooms, either in their fresh or processed forms, can be a new source of this vitamin. Hot-air dried mushrooms contained from 21.51 to 81.17 l g/g dw VD 2. White button mushroom is the richest in sterols (mainly ergosterol), precursor form of VD 2.[13] Mushrooms are low in calorie, cholesterol, fat, and sodium so they could be used to develop a healthy diet for diabetic patients.[14]
The effect of WBM on healthy individuals or those with metabolic syndrome has investigated in previous studies, however, type 2 diabetes has not been evaluated yet.[15],[16] In addition, the effect of WBM on glycemic indices in humans with type 2 diabetes has not been studied before.[5],[10] The most common and cheapest methods of dehydration mushrooms are hot-air drying at a temperature from 40°C to 70°C.[13] To our knowledge, this is the first time that the HAD-WBM effect has been tested in humans.[17] Previous studies have mainly investigated the extract, fresh or freeze-dried form of the WBM.[10] Hence, this study examined the effect of HAD-WBM on glycemic indices, lipid profile, inflammatory biomarkers, and antioxidant capacity in patients with T2DM.
| Methods | | |
Study design
This study was a randomized, placebo-controlled, double-blind clinical trial that assessed the effect of Hot Air-dried White Button Mushroom (HAD-WBM) powder on glycemic status, lipid profile, inflammatory markers, and total antioxidant capacity (TAC) in T2DM patients. This study was conducted from April to July 2017.
Participants
This study was conducted in Golestan Hospital, Ahvaz, Iran. Eligible patients were adults aged 20–50 with type 2 diabetes. Inclusion criteria included age = 20–50 years with body mass index (BMI) = 20–35 kg/m2, Type 2 diabetes for at least 2 years, use blood glucose medication for at least 6 months (no insulin), not taking nutritional supplements within the past 3 weeks. Pregnancy, lactation, cigarettes, weight loss in the last 6 months, allergy to mushroom, taking mushroom more than once or twice a week, having certain medical conditions, taking certain medications, changes in drug usage, taking fiber, omega-3, vitamin, and antioxidant supplements during the study were defined as exclusion criteria.
Forty-four patients with type 2 diabetes (18 males and 26 females; 20–50 years) were recruited.
Intervention
The intervention group receives 16 g HAD_WBM powder daily for 8 weeks. Patients in the control group received 16 g/d cornstarch for 8 weeks as well. The powder was taken at lunch in the raw form with salads, yogurt, or water. Three participants refused to continue the intervention because of gastrointestinal complaints, hypoglycemia, and the unpleasant taste of the powder. Therefore, the data of the 41 participants were analyzed (n = 22 intervention group, n = 19 placebo group).
The study protocol was approved by the Ethics Committee of Ahvaz Jundishapur University of Medical Sciences and registered on the Iranian Clinical Trials website (No. IRCT2017062534760N1). Written consent was received from all participants in the study.
Outcome
The primary outcomes of interest were FTA, fasting blood sugar (FBS), insulin, homeostatic model assessment for insulin resistance (HOMA-IR), and secondary outcomes were triglyceride (TG), low-density lipoprotein (LDL)-C, high-density lipoprotein (HDL)-C, very-LDL (VLDL)-C, cholesterol, high-sensitivity C-reactive protein (hs-CRP), IL-6, and TAC.
Dietary intake and physical activity
To evaluate the dietary intake, a 3-day 24-h dietary recall questionnaire (two weekdays and a weekend) was filled out at the beginning and end of the study. Nutritional analysis was performed by Nutritionist 4 software (Version 7; N-squared computing, OR, USA) which was altered for Iranian foods.
In this study, a short version of the International Physical Activity Questionnaire (IPAQ) was used to assess the physical activity level. This questionnaire included seven questions about the frequency and timing of physical activity of participants over the past 7 days. IPAQ short forms were completed by interview for illiterate subjects or self-report for the literate. The IPAQ scoring protocol assesses the physical activity of participants in four levels of vigorous intensity, moderate intensity, walking, and sitting.[18] The scores of the short IPAQ were converted to MET-min/wk. One MET equals the amount of oxygen the body uses at rest sitting, which approximates 3.5 mL O2/kg/min.[19] The number of minutes for each activity class was multiplied by the number of days per week and specific MET a score for each activity (8 for vigorous, 4 for moderate, and 3.3 for walking). By adding up of them totals MET score was obtained for each subject. Total MET scores 0-<600 considered as a mild activity, 600-<3000 as moderate activity, and ≥3000 as severe activity.[18]
Preparation of white button mushroom powder
I HAD-WBM was donated by the Agricultural Development Company of Dezful, Iran. The sliced fruit body of the fresh mushroom (4 mm thick) was placed under hot and dry air (10,000 m3/ton) for 8 h at 60°C. Then It was ground. The nutrient composition of HAD-WBM (as intervention) and cornstarch powder (as placebo) is shown in [Table 1]. Pre-packed powder of HAD-WBM and cornstarch was given to the participants. The supplements and placebo are similar in terms of organoleptic characteristics (color, odor, and shape). | Table 1: Nutrient composition of hot air-dried - white button mushroom and cornstarch powder
Click here to view |
Anthropometric and biochemical assessment
We measured weight, height (for calculating BMI), using seca scale with a precision of 0.1 kg and a wall height meter with a precision of 0.1 cm, respectively.
After 12 h of fasting overnight, venous blood (10 ml) was taken from all patients at the baseline and 8 weeks after the intervention. Serums were rapidly centrifuged (3000 rpm for 10 min) and stored at-80°C until biomarkers were measured. The enzyme-linked immunosorbent assay (ELISA) kits were used for assessment of insulin (mono binds, USA), fructosamine (Zellbio GmbH, Germany), IL-6 (IBL Co., Ltd. Germany), hs-CRP (LDN, Germany), and TAC (GmbH, Germany). ELx 808, Biotec, America ELISA reader was used for ELISA analysis. Fasting blood glucose (glucose oxidase method), serum TG (enzyme colorimetric method), total cholesterol, LDL-C, and HDL-C (enzymatic photometric method) were assessed by Pars Azmoon Co., Tehran, Iran, kits. An autoanalyzer (Biotecnica BT 3000 PLUS, Italy) was used for the evaluation of all the above-mentioned variables. The HOMA-IR index was calculated by fasting glucose (mmol/l) × fasting insulin (μm/ml)/22.5.[20]
Sample size
Two-mean comparison formula was used to determine sample size (α = 0.01, β = 0.1, and power = 90%). Based on LDL (113.6 ± 12.2 vs. 101.1 ± 5.5) as the primary outcome of previous studies.[21] The primary sample size was equal to two groups of 17 (34 in total). According to the probability of falling of about 30% of the subjects during the study, the final sample size was estimated to be 22 in each group (44 in total).
Blinding
Both the patients and the medical staff, especially the person evaluating the outcome were kept uninformed from the type of medication assigned to each individual. From the beginning of the study, all patients who met the inclusion criteria and did not meet the exclusion criteria were selected as the sample until the final sample size was reached. Statistician generated the random allocation sequence. A nutritionist who was unaware of the study program and code definition enrolled participants and assigned participants to interventions. The patients were randomly allocated into the two groups (intervention and placebo) according to random permuted block procedure (block design) based on the combined analysis. In the present study, all patients were assigned to six groups with four codes A and B in two steps (first step; AABB, BBAA, ABAB, BABA, ABBA, BABA, second step; AABB, BBAA, ABAB, BABA, ABBA).
Statistical analysis
All data were analyzed using SPSS 23 software (IBM/SPSS Inc., Chicago, IL, USA). The intention-to-Treat analysis method was used for the analysis. A Shapiro-Wilks test was used to evaluate the normality of the data distributions. The Chi-squared test was used for comparing categorical data between two groups. Independent sample t-test for variables with normal distribution or Mann–Whitney U tests for variables with nonnormal distribution was used to compare quantitative variables between two groups. A comparison of the mean values before and after treatment in each group was performed with either paired t-test or Wilcoxon signed-rank test for normal data and non-normal data, respectively. The significance level of all tests was considered to be < 0.05.
| Results | | |
Recruitment, enrolment, and randomization
Forty-one patients (n = 19 and 22 in the HAD-WBM and control group, respectively) completed the trial. The summary of recruitment, enrolment, and randomization of patients is shown in [Figure 1].
Baseline characteristics
The basic characteristics of the participants are shown in [Table 2]. At the beginning of the study, there was no significant difference between the two groups in terms of age, duration of diabetes, height, BMI, waist-to-hip ratio, and physical activity (P ≥ 0.05) [Table 2]. Furthermore, there was no significant difference between the type and amount of drug used between groups (data not presented) (P ≥ 0.05).
Diet analysis
No significant differences were observed in the dietary data including energy (1852 vs. 1588, P = 0.25), carbohydrate (244.28 ± 88.36 vs. 234.32 ± 95.20, P = 0.53), fat (61.29 ± 22.41 vs. 50.89 ± 18.74, P = 0.15), cholesterol (300.06 ± 222.60 vs. 296.05 ± 246.20, P = 0.57), fiber (11.89 ± 6.03 vs. 11.14 ± 93.00, P = 0.52), vitamin E (2.42 ± 1.63 vs. 2.02 ± 1.07, P = 0.27), vitamin C (82.56 ± 81.00 vs. 73.37 ± 44.34, P = 0.42) and zinc (7.48 ± 2.47 vs. 6.12 ± 1.65, P = 0.07) between the two groups at baseline [Table 3]. In addition, no significant differences were observed in the dietary data (energy, carbohydrate, fat, cholesterol, fiber, Vitamin E, Vitamin C, and zinc) at the end of the study (P ≥ 0.05) [Table 3].
Serum parameters
Glycemic indices
This study showed a significant reduction in serum fructosamine concentration in the HAD-WBM group compared with the cornstarch group (-0.228 ± 0.36 vs. 0.03 ± 0.38; P = 0.022). Moreover, in the HAD-WBM group, fructosamine was reduced significantly post-intervention compared to baseline (From 1.34 ± 0.23 to 1.11 ± 0.26 mmol/l; P = 0.007). However, no significant difference was noted for corn starch group compared to baseline (from 1.26 ± 0.28 to 1.30 ± 0.30 mmol/l; P = 0.665) [Table 4]. After 8 weeks of intervention, mean concentration of fasting insulin and FBS were not significantly different between two groups (−1.27 ± 4.47 vs. −0.52 ± 6.19 μIU/ml; P = 0.649, −28.00 ± 42.46 vs. −15.95 ± 48.64 mg/dl; P = 0.387, respectively). However, a significant within-group reduction (from 180.09 ± 60.86 to 152.09 ± 58.39 mg/dl; P = 0.006) was observed for FBS in the HAD-WBM group. In the control group, no significant within-group difference was observed for FBS (from 185.77 ± 73.36 to 169.82 ± 66.01 mg/dl; P = 0.139). At the end of the intervention, there were no significant differences in fasting insulin levels compared to baseline in both groups (P ≥ 0.05) [Table 4]. | Table 4: Metabolic variables before and after intervention in both groups
Click here to view |
In the HAD-WBM group, insulin resistance (HOMA-IR) reduced significantly at the end of the study (From 4.92 ± 2.09 to 3.81 ± 1.87; P = 0.016), but it was not significantly different between the two groups (−1.10 ± 1.97 vs. −0.81 ± 3.44; P = 0.733). There were no statistically significant differences in HOMA_IR in the control group compared to baseline (from 4.90 ± 4.13 to 4.09 ± 2.15; P = 0.279) [Table 4].
Lipid profile
In this study, after 8 weeks, serum LDL-C concentration decreased significantly in the intervention group compared with the control group (-13.05 ± 20.67 vs. 0.81 ± 21.79; P = 0.041). There were no statistically significant differences in LDL-C in the control group compared to the baseline (from 67.14 ± 27.00 to 67.95 ± 29.32 mg/dl; P = 0.867). However, serum LDL-C concentration in HAD_WBM group was significantly lower than the baseline (from 73.86 ± 28.19 to 60.81 ± 28.32 mg/dl; P = 0.009) [Table 4]. At the end of the intervention, TG, HDL-C, and VLDL was not significantly different between the two groups (P = 0.415, P = 0.655, and P = 0.361, respectively). However, the HAD-WBM group had lower TG (−11.09 ± 54.1), lower VLDL (−2.38 ± 10.73), and higher HDL-C (0.68 ± 5.52) compared with the baseline (P = 0.347, P = 0.309, P = 0.569 respectively). Moreover, in the corn starch group, TG, HDL-C, and VLDL was not significantly different post-intervention compared to baseline (From 206.41 ± 102.27 to 214.14 ± 96.94 mg/dl; P = 0.698, from 46.64 ± 9.39 to 48.23 ± 11.27 mg/dl; P = 0.344 and from 41.02 ± 20.07 to 42.84 ± 19.33 mg/dl; P = 0.648; respectively) [Table 4]. Regarding serum levels of total cholesterol, there was only a decreasing trend (-14.40 ± 28.93 vs. 2.23 ± 25.73; P = 0.05) in the intervention group compared with the control group. Within-group reduction of total cholesterol in the intervention group was significant (from 152.14 ± 39.24 to 137.73 ± 37.60 mg/dl; P = 0.029) [Table 4]. However, after eight weeks in the corn starch group, serum levels of total cholesterol were not significantly different compared to baseline (From 151.95 ± 39.21 to 154.18 ± 42.80 mg/dl; P = 0.689) [Table 4].
Inflammatory biomarkers and total antioxidant capacity
There was no significant difference in TAC, hs-CRP and IL-6 between the intervention and control groups post intervention (P = 0.207, P = 0.708, and P = 0.360, respectively). At the end of the intervention, there were no significant differences in serum TAC, hs-CRP, and IL-6 levels compared to baseline in both groups (all P ≥ 0.05) [Table 4].
Side effects
Due to abdominal discomfort, appetite loss, and unpleasant taste of HAD-WBM powder three participants were excluded during the intervention. Thus, the present study does not unequivocally show serious adverse events but suggests that this matter needs to be considered carefully before HAD-WBM supplementation can be broadly advocated.
| Discussion | | |
Effect of hot air-dried white button mushroom on primary outcome: Glycemic indices
In our study, the consumption of HAD-WBM for 8 weeks by diabetic patients caused a significant within-group decrease in serum levels of FBS and HOMA-IR. In addition, the serum concentration of fructosamine, both within and between groups, decreased significantly. According to our findings, it was the first time that fructosamine concentration was measured in the intervention with the mushrooms. Blood levels of fructosamine are more fluctuating than HbA1C, and in diabetic and nondiabetic patients reflect better for rapid and varied blood-glucose changes. Hence, it responds to treatment faster and may be a better marker for glycemic control than HbA1C.[22] Based on our knowledge, there is no study on the effects of WBM on glycemic indices in diabetic patients. Our study compared with previous studies (on subjects with metabolic syndrome or obese subjects) showed further changes in less time. Therefore, people who have a higher level of glucose disorder are more suitable options to get the best out of complementary treatments with medicinal mushrooms. However, the dosage and type of mushroom product prescribed (raw form, cooked, freeze-dried, Air-dried, Aqueous/alcohol extracts) can also affect its health effects.
In the study conducted by Calvo et al., on adults with metabolic syndrome, there was no significant change in insulin resistance or glucose metabolism by administering 100 gr/day of fresh WBM for 16 weeks.[15] While FBS significantly improved in 1-year mushroom replacement with meat (8 ounces 3 days a week) in obese adults.[23] Hsu et al. reported that low-dose of mushroom agaricus blazei Murill (1500 mg daily) for 12 weeks improves insulin resistance among subjects with T2DM.[24] Although, in their study, the mushroom was intervened in combination with metformin and gliclazide. In a clinical trial, short-term effects of oyster mushroom evaluated in diabetic subjects. The results have shown that 24-day intervention with mushrooms significantly reduced blood pressure, plasma glucose, and lipid profile.[25] Recently, Sun and Niu et al. reported that consuming low-dose of mushrooms (100 g/day) can control Pregnancy-induced hypertension and diabetes.[26] Along with our study, in the study of the effect of freeze-dried WBM in diabetic rats, there was a significant decrease in plasma glucose concentration after 3 weeks of intervention (24.7%).[10] Moreover, WBM aqueous extracts in diabetic rats significantly decreased serum glucose levels (29.68%) and increased serum insulin levels (78.50%).[5] In diabetes expression of tumor necrosis factor-alpha (TNF-α) and interleukin (IL)-6 is increased by reducing adiponectin (anti-inflammatory hormone) production and increasing pro-inflammatory cytokines production, all of which enhance insulin resistance.[27] Subclinical systemic inflammation in Type 2 diabetes is associated with beta-cell inflammation, which disrupts beta-cell function.[28] In mushrooms, beta-glucan-rich polysaccharides decrease insulin resistance by increasing GLUT-4 (insulin-responsive glucose transporter) and anti-atherogenic hormone adiponectin and downregulation of NF-KB expression (regulation of the genes of proteins involved in immune and inflammatory responses including IL-6).[27],[29],[30] In addition, polysaccharides prevent the degradation of pancreatic beta cells by reducing the expression of NOS and reducing NO production.[31] Increasing expression of insulin, glucokinase, and GLUT-1 and increasing the proliferation of beta cells leads to reduce blood glucose concentrations and increases glucose tolerance which are the effects of Agaricus Bisporus lectins (ABL). This is indicating the potential effect of ABL in preventing or treating diabetes.[32]
Effect of hot air-dried white button mushroom on secondary outcomes: Lipid profile, inflammatory biomarkers, and total antioxidant capacity
In our study, positive changes in serum levels of lipid profiles were found in type 2 diabetic patients. The intervention group showed a significant decrease in serum LDL-C levels compared to the corn starch group, but the serum level of total cholesterol showed a tendency to decrease, which was not statistically significant. Moreover, the intervention group showed a higher decrease in mean concentrations of TG and VLDL, and a higher increase in HDL-C, but not significant. Unlike our study, previous clinical studies after 16 weeks of intervention did not show any significant changes in lipid profile.[15] In the study of the postprandial effect of AB on healthy participants, there was no significant difference in the lipid profile however, supplementation led to a decreasing trend in TG.[16] However, long-term studies showed the positive effect of WBM intervention on improving LDL, TG, and HDL.[22] In agreement with our study, in the study of Wistar rats, the serum levels of total lipid and TG decreased significantly with WBM powder (dried in an oven at 60°C for 12 h).[17]
AB contained 565/4 mg/kg lovastatin (an inhibitor of HMG-COA reductase), which reduces serum and hepatic levels of cholesterol.[33] Furthermore, WBM sterol (ergosterol) is a hypocholesterolemia component that disrupts cholesterol transport through Caco2 monolayers.[34] In addition, the fermentation of dietary mushroom's fiber produces short-chain fatty acids, including propionate, which combined with beta-glucans lead to inhibit the synthesis of cholesterol. Moreover, reduces cholesterol entry into the intestinal-liver cycle by binding to bile acids. Finally, it increases the secretion of bile acid in the intestine, increases the conversion of hepatic cholesterol to bile acid, and ultimately reduces circulating cholesterol.[35]
Despite a within-group decrease in the mean concentration of hs-CRP and IL-6 levels and an increase in serum TAC level, these changes were similar between the two groups. So, the results of this study failed to support the anti-inflammatory and antioxidant effects of HAD-WBM in patients with type 2 diabetes. No significant changes between groups may be due to the small sample size so studies with more participants may change the results.
In accordance with our study, Beelman et al. suggest that freeze-dried AB (Brown crimini) did not have any significant effect on hs-CRP in different doses and with increasing consumption of the mushroom, ORAC decreased significantly.[16] In the other study by Poddar et al., in the 1-year replacement of the mushroom with meat, hs-CRP was improved, but IL-6 did not change significantly.[23] In a clinical trial, the results showed that the use of AB alpha-glucan (5 g glucan/day) reduced TNFα Production by 69% compared with the control group, but did not have any effect on IL-1 β And IL-6.[36] A study on THP-1 cells of human monocytes, showed that the semi-enriched AB extract stimulates the production of enzymes and inflammatory cytokines.[37]
Mushrooms are an excellent source of antioxidants, especially ergothioneine, exopolysaccharides, the total polyphenol, copper, zinc, iron, and manganese.[38],[39] In the mushrooms, ergosterol and ergosterol peroxidase can also inhibit the inflammation process, while natural anti-inflammatory substances are isolated only from certain types of mushrooms, and only certain species of the mushroom show the significant anti-inflammatory effect.[35] The chitosan in the mushrooms also interferes with inflammatory disorders by reducing the lipid absorption of food, decreasing fat mass, reducing secretion, and abnormal saving of fat in the liver and muscle.[40] AB exopolysaccharides, through the removal of hydroxyl radicals and superoxides, exert their anti-inflammatory effects.[41] Furthermore, the fucogalactan from AB reduces inflammation by inhibiting COX-2 proteins and inhibiting the expression of iNOS.[42]
Limitations
The limitation of the study was the short intervention period, so that intervention period longer than 8 weeks in the future studies may alter the results. Thus, longer studies are recommended.
| Conclusion | | |
To our knowledge, this is the first study that has examined the association between mushroom consumption and T2DM. Given the wide popularity of mushrooms and the growing interest in their potential clinical effects, studies addressing the limitations of the present study are warranted to further evaluate the relationship between mushroom consumption and health. Studies with long-term mushroom consumption, more frequency and more amount of mushroom consumption, and potential dose-response association of mushroom consumption is needed to examine. The mushrooms and their extracts are generally tolerable or even have no side effects.[27] The edible mushrooms can be used with other therapy for more effective results in type 2 diabetes.
Acknowledgments
This study has been funded by the Ahvaz Jundishapur University of Medical Sciences and registered under number NRC-9608. Mr. Reza Sohrabi Kabi is appreciated for his kind help in all stages of the study. The authors are grateful to Mr. Ayashi for performing ELISA tests. Thanks to all the staff of the specialized clinic of Golestan hospital at Ahvaz, Iran.
Financial support and sponsorship
Financial support was provided by Ahvaz Jundishapur University of Medical Sciences.
Conflicts of interest
There are no conflicts of interest.
| References | | |
| 1. | American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 2014;37 Suppl 1:S81-90.  |
| 2. | van Sloten TT, Sedaghat S, Carnethon MR, Launer LJ, Stehouwer CD. Cerebral microvascular complications of type 2 diabetes: Stroke, cognitive dysfunction, and depression. Lancet Diabetes Endocrinol 2020;8:325-36. |
| 3. | Alipour M, Rostami H, Parastouei K. Association between inflammatory obesity phenotypes, FTO-rs9939609, and cardiovascular risk factors in patients with type 2 diabetes. J Res Med Sci 2020;25:46. [Full text] |
| 4. | Kim HJ, An SY, Han SJ, Kim DJ, Hong CH, Kim YH, et al. The association of diabetes duration and glycemic control with depression in elderly men with type 2 diabetes mellitus. J Res Med Sci 2019;24:17. [ PUBMED] [Full text] |
| 5. | Ogurtsova K, da Rocha Fernandes JD, Huang Y, Linnenkamp U, Guariguata L, Cho NH, et al. IDF Diabetes Atlas: Global estimates for the prevalence of diabetes for 2015 and 2040. Diabetes Res Clin Pract 2017;128:40-50. |
| 6. | Alipour M, Malihi R, Hosseini SA, Abbasnezhad A, Ghavami A, Shahmohammadi HA, et al. The effects of catechins on related risk factors with type 2 diabetes: A review. Prog Nutr 2018;20:12-20. |
| 7. | Hosseini SA, Ghaedi E, Zakerkish M, Ghadiri A, Ashtary-Larky D, Safari M, et al. Effects of ginseng extract on chemerin, apelin and glycemic biomarkers in type 2 diabetic patients. Indian J Physiol Pharmacol 2017;61:152-8. |
| 8. | Roupas P, Keogh J, Noakes M, Margetts C, Taylor P. The role of edible mushrooms in health: Evaluation of the evidence. J Funct Foods 2012;4:687-709. |
| 9. | Atila F, Owaid MN, Shariati MA. The nutritional and medical benefits of Agaricus bisporus: A review. J Microbiol Biotechnol Food Sci 2017;7:281. |
| 10. | Jeong SC, Jeong YT, Yang BK, Islam R, Koyyalamudi SR, Pang G, et al. White button mushroom ( Agaricus bisporus) lowers blood glucose and cholesterol levels in diabetic and hypercholesterolemic rats. Nutr Res 2010;30:49-56. |
| 11. | Muszyńska B, Kała K, Rojowski J, Grzywacz A, Opoka W. Composition and biological properties of Agaricus bisporus fruiting bodies – A review. Polish J Food Nutr Sci 2017;67:173-82. |
| 12. | Aljack HA, Abdalla MK, Idris OF, Ismail AM. Vitamin D deficiency increases risk of nephropathy and cardiovascular diseases in type 2 diabetes mellitus patients. J Res Med Sci 2019;24:47. [ PUBMED] [Full text] |
| 13. | Sławińska A, Fornal E, Radzki W, Skrzypczak K, Zalewska-Korona M, Michalak-Majewska M, et al. Study on vitamin D 2 stability in dried mushrooms during drying and storage. Food Chem 2016;199:203-9. |
| 14. | Friedman M. Mushroom polysaccharides: Chemistry and antiobesity, antidiabetes, anticancer, and antibiotic properties in cells, rodents, and humans. Foods 2016;5:80. |
| 15. | Calvo MS, Mehrotra A, Beelman RB, Nadkarni G, Wang L, Cai W, et al. A retrospective study in adults with metabolic syndrome: Diabetic risk factor response to daily consumption of Agaricus bisporus (White Button Mushrooms). Plant Foods Hum Nutr 2016;71:245-51. |
| 16. | Weigand-Heller AJ, Kris-Etherton PM, Beelman RB. The bioavailability of ergothioneine from mushrooms ( Agaricus bisporus) and the acute effects on antioxidant capacity and biomarkers of inflammation. Prev Med 2012;54 Suppl: S75-8. |
| 17. | Goyal R, Grewal R. Changes in lipid profile of rats fed with Agaricus bisporus (white button) mushroom. Nutr Food Sci 2017;47:288-96. |
| 18. | IPAQ Research Committee. Guidelines for Data Processing and Analysis of the International Physical Activity Questionnaire (IPAQ)–Short and Long Forms. [Online]. 2005. Available from: URL: http://www.ipaq.ki.se/scoring. pdf. [Last accessed on 2009 Jun 10]. |
| 19. | Franklin BA, Brinks J, Berra K, Lavie CJ, Gordon NF, Sperling LS. Using metabolic equivalents in clinical practice. Am J Cardiol 2018;121:382-7. |
| 20. | Gayoso-Diz P, Otero-González A, Rodriguez-Alvarez MX, Gude F, García F, De Francisco A, et al. Insulin resistance (HOMA-IR) cut-off values and the metabolic syndrome in a general adult population: Effect of gender and age: EPIRCE cross-sectional study. BMC Endocr Disord 2013;13:47. |
| 21. | Chang JH, Kim MS, Kim JY, Choi WH, Lee SS. Effects of mushroom supplementation on blood glucose concentration, lipid profile, and antioxidant enzyme activities in patients with type 2 diabetes mellitus. J Nutr Health 2007;40:327-33. |
| 22. | Shohat N, Tarabichi M, Tischler EH, Jabbour S, Parvizi J. Serum fructosamine: A simple and inexpensive test for assessing preoperative glycemic control. J Bone Joint Surg Am 2017;99:1900-7. |
| 23. | Poddar KH, Ames M, Hsin-Jen C, Feeney MJ, Wang Y, Cheskin LJ. Positive effect of mushrooms substituted for meat on body weight, body composition, and health parameters. A 1-year randomized clinical trial. Appetite 2013;71:379-87. |
| 24. | Hsu CH, Liao YL, Lin SC, Hwang KC, Chou P. The mushroom Agaricus Blazei Murill in combination with metformin and gliclazide improves insulin resistance in type 2 diabetes: A randomized, double-blinded, and placebo-controlled clinical trial. J Altern Complement Med 2007;13:97-102. |
| 25. | Khatun K, Mahtab H, Khanam PA, Sayeed MA, Khan KA. Oyster mushroom reduced blood glucose and cholesterol in diabetic subjects. Mymensingh Med J 2007;16:94-9. |
| 26. | Sun L, Niu Z. A mushroom diet reduced the risk of pregnancy-induced hypertension and macrosomia: A randomized clinical trial. Food Nutr Res 2020;64:10.29219/fnr.v64.4451. |
| 27. | Kanagasabapathy G, Chua K, Malek S, Vikineswary S, Kuppusamy U. AMP-activated protein kinase mediates insulin-like and lipo-mobilising effects of β-glucan-rich polysaccharides isolated from Pleurotus sajor-caju (Fr.), Singer mushroom, in 3T3-L1 cells. Food Chem 2014;145:198-204. |
| 28. | Daniele G, Mendoza RG, Winnier D, Fiorentino T, Pengou Z, Cornell J, et al. The inflammatory status score including IL-6, TNF-α, osteopontin, fractalkine, MCP-1 and adiponectin underlies whole-body insulin resistance and hyperglycemia in type 2 diabetes mellitus. Acta Diabetol 2014;51:123-31. |
| 29. | Kanagasabapathy G, Kuppusamy UR, Abd Malek SN, Abdulla MA, Chua KH, Sabaratnam V. Glucan-rich polysaccharides from Pleurotus sajor-caju (Fr.) Singer prevents glucose intolerance, insulin resistance and inflammation in C57BL/6J mice fed a high-fat diet. BMC Complement Altern Med 2012;12:261. |
| 30. | Vincent M, Philippe E, Everard A, Kassis N, Rouch C, Denom J, et al. Dietary supplementation with Agaricus blazei murill extract prevents diet-induced obesity and insulin resistance in rats. Obesity 2013;21:553-61. |
| 31. | Lee BR, Lee YP, Kim DW, Song HY, Yoo KY, Won MH, et al. Amelioration of streptozotocin-induced diabetes by Agrocybe chaxingu polysaccharide. Mol Cells 2010;29:349-54. |
| 32. | Wang Y, Liu Y, Wang H, Li C, Qi P, Bao J. Agaricus bisporus lectins mediates islet β-cell proliferation through regulation of cell cycle proteins. Exp Biol Med 2012;237:287-96. |
| 33. | Chen SY, Ho KJ, Hsieh YJ, Wang LT, Mau JL. Contents of lovastatin, γ-aminobutyric acid and ergothioneine in mushroom fruiting bodies and mycelia. LWT Food Sci Technol 2012;47:274-8. |
| 34. | Gil-Ramírez A, Ruiz-Rodríguez A, Marín FR, Reglero G, Soler-Rivas C. Effect of ergosterol-enriched extracts obtained from Agaricus bisporus on cholesterol absorption using an in vitro digestion model. J Funct Foods 2014;11:589-97. |
| 35. | Molz P, Ellwanger J, Prá D, Franke S. Mushrooms: Biological characterization, antioxidant properties and interactions with human health. New York: Nova Science Publishers; 2014. p. 75-92. |
| 36. | Volman J, Mensink R, Van Griensven L, Plat J. Effects of α-glucans from Agaricus bisporus on ex vivo cytokine production by LPS and PHA-stimulated PBMCs; a placebo-controlled study in slightly hypercholesterolemic subjects. Eur J Clin Nutr 2010;64:720. |
| 37. | Smiderle FR, Ruthes AC, van Arkel J, Chanput W, Iacomini M, Wichers HJ, et al. Polysaccharides from Agaricus bisporus and Agaricus brasiliensis show similarities in their structures and their immunomodulatory effects on human monocytic THP-1 cells. BMC Complement Altern Med 2011;11:58. |
| 38. | Ghahremani-Majd H, Dashti F. Chemical composition and antioxidant properties of cultivated button mushrooms ( Agaricus bisporus). Hortic Environ Biotechnol 2015;56:376-82. |
| 39. | Reis FS, Martins A, Barros L, Ferreira IC. Antioxidant properties and phenolic profile of the most widely appreciated cultivated mushrooms: A comparative study between in vivo and in vitro samples. Food Chem Toxicol 2012;50:1201-7. |
| 40. | Neyrinck AM, Bindels LB, De Backer F, Pachikian BD, Cani PD, Delzenne NM. Dietary supplementation with chitosan derived from mushrooms changes adipocytokine profile in diet-induced obese mice, a phenomenon linked to its lipid-lowering action. Int Immunopharmacol 2009;9:767-73. |
| 41. | Mao Y, Mao J, Meng X. Extraction optimization and bioactivity of exopolysaccharides from Agaricus bisporus. Carbohydr Polym 2013;92:1602-7. |
| 42. | Ruthes AC, Rattmann YD, Malquevicz-Paiva SM, Carbonero ER, Córdova MM, Baggio CH, et al. Agaricus bisporus fucogalactan: Structural characterization and pharmacological approaches. Carbohydr Polym 2013;92:184-91. |
[Figure 1]
[Table 1], [Table 2], [Table 3], [Table 4]
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