Effects of different intensity aerobic exercise on intestinal flora and gastrointestinal hormones in type 2 diabetic rats

Abstract

To examine the impact and mechanisms of the aerobics exercise on gut flora and gastrointestinal hormones in type 2 diabetes rats. Methods Adult male SD rats aged 8 weeks were divided into 5 groups at random ( $n=$ 10): a peaceful comparison group (N), a diabetic comparison group (D), a diabetic low-intensity exercise group (LD), a diabetic middle-intensity exercise group (MD), and a diabetes highintensity exercise group. (HD). The rat groups LD, MD, and HD performed aerobic exercise five times per week for a total of 6 weeks and compared general condition, blood glucose, blood lipids, insulin, leptin, gastrin (GAS) and motilin ( MOT), gastrointestinal motility, and intestinal flora. Results The levels of insulin, leptin, total cholesterol, triglycerides, E. coli, LDL-cholesterol, LDL-cholesterol, insulin, and gastric residual rate were significantly different from group N. Conclusion: Type 2 diabetic rats have gut flora imbalance and gastrointestinal hormone changes. Aerobic exercise with different intensity can alleviate gastrointestinal hormone imbalance and intestinal flora imbalance in type 2 diabetes rats, and the impact of moderate intensity exercise is the strongest.

Keywords

Aerobic exercise type 2 diabetes;intestinal flora gastrointestinal hormones

1. Introduction

Many studies have demonstrated the close connection between intestinal flora and host health as well as the fact that disruptions in the dynamic balance of the gastrointestinal flora are the primary initiators of metabolic disorders [1]. One of the most prevalent consequences of diabetes is poor glucolipid metabolism, which also serves as a key pathophysiological foundation for chronic complications of diabetes, according to studies [2], and host glucolipid metabolism can be significantly regulated by the gut flora [3]. The direction of type 2 diabetes prevention and treatment research is now focusing on the gut flora as a new target.

Several studies have shown that exercise can significantly regulate intestinal flora, perhaps as a result of improved glucolipid metabolism [4]. The results of numerous animal studies as well as experimental studies in humans confirm that exercise regulates the abundance of intestinal flora. There is an influence on the structure of intestinal flora as well as on metabolic disorders such as glucose and lipids and on the process of resistance to inflammatory factors [5]. Exercise, a relatively safe non-pharmacological treatment, has a positive impact on the development and prevention of diabetes, but studies on the relationship between exercise and type 2 diabetes gut flora are less well-reported, and the precise mechanism is unclear. Today, prevention and control of diabetes and its complications remain a significant challenge. As a result, we were able to recreate type 2 diabetes mellitus in rats for this investigation, and we subsequently used several exercise modalities as an intervention.In order to establish an experimental foundation for the function of exercise on the intestinal flora of rats with type 2 diabetes mellitus and the potential mechanisms, as well as to provide a basis for the prevention and treatment of type 2 diabetes mellitus, the changes of exercise on glucose and lipid metabolism, intestinal flora, and gastrointestinal hormones of the rats were compared with the control group after the experiment was completed. This is a summary of the study’s findings.

2. Experimental procedure

2.1 Main reagents and instruments

Main reagents: blood glucose and lipid kits (Nanjing Jiancheng Institute of Biotechnology), serum GAS, MOT and leptin assay kits (Shanghai Xitang Biotechnology Co., Ltd.), streptozotocin (STZ) (purchased from Sigma).

Main instruments: Toshiba automatic biochemical analyzer, DU530 UV spectrophotometer (BECKMAN).

2.2 Experimental animal grouping and the establishment of its diabetes model

At Xi’an Jiaotong University’s Experimental Animal Management Center, fifty male SD rats weighing (20020) g were purchased. The high-fat diet consisted of a food with 2% cholesterol, 10% lard, and 0.5% sodium cholate, while the usual diet was a typical rat diet. We randomly divided all the rats into five groups ( $n=$ 10) after 1 day of acclimation feeding: a peaceful comparison group (N), a diabetic comparison group (D), diabetes of low-intensity aerobic exercise group (LD), diabetes of middle-intensity aerobic exercise group (MD), and diabetes of high-intensity aerobic exercise group (HD). Rats in group N received standard diet without any special care while rats in groups LD, MD, HD, and D were given high-fat food for two months after receiving a single intraperitoneal injection of 35 mg/kg STZ following a 16-hour fast [8], STZ was dissolved in 0.1 mmol/L raffinate buffer, pH $=$ 4.2, ready to use, and blood was collected from the tail vein 7 d after injection to test the blood glucose level, the blood glucose level exceeded 16.7 mmol/L and lasted for three weeks, for the adult rats.

2.3 Aerobic exercise program

The rats in the LD, MD and HD groups of the exercise intervention were subjected to aerobic exercise on a running platform for 6 weeks with a starting speed of 8, 18 and 28 m/min, respectively, and an incline of 5 degrees, with 5 d of continuous exercise per week and 2 days of rest, with each exercise lasting 30 min.

2.4 General index observation records and sample collection

During the experiment, the general physiological and mental conditions of the rats in each group were observed and recorded daily until the experiment was completed. After the final bout of aerobic activity, blood was drawn from six randomly chosen rats from each group. To examine the biochemical indices, 4 ml of blood from the eyes was taken, centrifuged, and stored at $-$ 20^∘C. The supernatant was also kept there.

2.5 Measurement of gastric emptying rate and intestinal propulsion rate

The remaining four rats in each group were fasted for one day following the conclusion of the previous experiment, and then the prepared food paste was given at a rate of 10 ml/kg. The rats were then killed 30 minutes after the food paste administration by dissection of the neck. After removing the stomach, weigh the entire weight of the stomach, then open the stomach alongside the greater curvature of the stomach, and the remains inside were then measured.

The specific measurement method of intestinal advancement rate: take out all the intestines of the above-mentioned executed rats, take a piece of pre-prepared white paper, lay it naturally flat on it, and measure from the pylorus of the intestine, first determine the intestine’s total length, and then gauge the food’s progress in distance, after the measurement of the two sets of data is completed, start to calculate the intestinal advancement rate (%) $=$ (distance of food advancement $\div$ full length of the intestine) $\times$ 100.

2.6 Biochemical indicators and their determination methods

Blood glucose was measured with an automated biochemical analyzer; serum gastrin (GAS), motilin (MOT), and leptin were measured with an enzyme immunoassay; triglycerides (TG) were measured with an GPO-PAP enzyme assay; The content of total cholesterol (TC) in serum was detected using the COD-PAP enzyme method; The contents of HDL-cholesterol in serum were measured by direct method;LDL-cholesterol; insulin content was measured using an enzyme-linked immunosorbent assay, and intestinal flora was examined both subjectively and quantitatively using the Lightoka method.

2.7 Statistical evaluation

After the experiment is completed, the mean $\pm$ standard deviation ( $x\pm s$ ) is used to represent the statistical results of all experimental data. SPSS 13.0 software is used for statistical analysis of the data. Two factor analysis of variance is selected for inter group comparison, and sample $t$ -test is selected for inter data comparison.

3. Results and discussion

3.1 Results

3.1.1 General situation analysis in rats of each group

The rats in the peaceful comparison group group had normal daily food intake, water consumption, and excretion; the rats in the diabetes group showed mental fatigue, decreased activity, dull fur, and significantly increased daily food intake, water intake and excretion; and the rats in the aerobic exercise group had significantly improved general physiological indices and their mental health. When compared to the diabetic group, rats in each aerobic exercise group significantly improved their mental state and other physiological indicators. The middle-intensity aerobic exercise group exhibited the greatest improvement.

3.1.2 Comparative analysis of changes in serum levels of GAS, MOT, and leptin in rats of each group

Table 1: After the experiment, Rats with diabetes have much greater amounts of leptin than rats without diabetes, GAS and MOT content in serum were remarkably decreased ( $P<$ 0.05, $P<$ 0.1); Leptin levels of rats in each aerobic exercise group were remarkably decreased than diabetic comparison group rats, GAS and MOT content in serum were remarkably increased( $P$ 0.05, $P$ 0.01), particularly in the middle-intensity group. The most notable modifications were seen in the middle-intensity group.

Table 1
Changes of GAS, MOT and Leptin levels in the serum of rats ( $\bar{r}\pm s$ , $n=$ 6)

Group	GAS/(pg $\cdot$ ml-1)		MOT/(pg $\cdot$ ml-1)		Leptin (ng/mL)
N	41.57	$\pm$ 4.36	138.79	$\pm$ 11.46	4.30	$\pm$ 0.071
D	28.17	$\pm$ 4.31^∗∗	100.39	$\pm$ 5.32^∗∗	6.07	$\pm$ 0.046^∗
LD	34.57	$\pm$ 3.08^{# #}	114.31	$\pm$ 4.43^{# #}	5.18	$\pm$ 0.077^#
MD	38.79	$\pm$ 5.25^{# #}	123.66	$\pm$ 10.30^{# #}	4.74	$\pm$ 0.024^{# #}
HD	32.99	$\pm$ 3.93^#	109.38	$\pm$ 9.06^#	5.83	$\pm$ 0.019^#

Note: Compared with peaceful comparison group, ^*P< 0.05, ^**P< 0.01; compared with diabetic comparison group, ^#P< 0.05, ^{# #}P< 0.01.

3.1.3 Comparison of the changes of blood glucose and lipid content in serum of rats in each group

According to Table 2, the diabetic rats had significantly higher blood glucose, TC, TG, and insulin levels than the peaceful comparison group after the experiment. The HDL-C levels were significantly lower ( $P$ 0.05, $P$ 0.01), and the LDL-C levels were higher, but there is no obvious difference ( $P>$ 0.05). The blood glucose, TC, TG, and insulin levels of the rats in each aerobic exercise group were remarkably decreased than diabetic comparison group rats. In both the LD and HD groups, the content of HDL-C shows a significant increase ( $P<$ 0.05, $P<$ 0.01), and the content of LDL-C shows decreased,but there was no significant statistical difference (A $P>$ 0.05). The changes in each index were particularly significant in the group that engaged in middle-intensity aerobic exercise.

Table 2
Analysis of changes in blood glucose and lipid levels in rat serum ( $\bar{r}\pm s$ , $n=$ 6)

Group	Blood glucose (mmol/L)		TC (mmol/L)		TG (mmol/L)		LDL-C (mmol/L)		HDL-C (mmol/L)		Insulin (mU/L)		Leptin (ng/mL)
N	7.46	$\pm$ 0.3	1.091	$\pm$ 0.008	0.612	$\pm$ 0.023	0.408	$\pm$ 0.021	0.566	$\pm$ 0.027	5.99	$\pm$ 0.76	4.30	$\pm$ 0.46
D	22.34	$\pm$ 4.1^**	2.427	$\pm$ 0.061^**	1.817	$\pm$ 0.040^*	0.602	$\pm$ 0.009	0.288	$\pm$ 0.038^*	14.34	$\pm$ 1.79^**	6.04	$\pm$ 0.027^*
LD	11.09	$\pm$ 3.7^{# #}	1.756	$\pm$ 0.065^#	1.038	$\pm$ 0.017^#	0.511	$\pm$ 0.023	0.40	$\pm$ 0.034^#	9.62	$\pm$ 1.37^#	5.27	$\pm$ 0.055^#
MD	9.87	$\pm$ 1.6^{# #}	1.106	$\pm$ 0.042^{# #}	0.765	$\pm$ 0.024^{# #}	0.498	$\pm$ 0.070^#	0.483	$\pm$ 0.025^#	7.46	$\pm$ 0.18^{# #}	4.94	$\pm$ 0.084^{# #}
HD	15.31	$\pm$ 4.3^#	1.917	$\pm$ 0.053^#	1.243	$\pm$ 0.047^#	0.561	$\pm$ 0.021	0.387	$\pm$ 0.034^#	10.37	$\pm$ 1.71^#	5.89	$\pm$ 0.015^{# #}

Note: Compared with peaceful comparison group, ^*P< 0.05, ^**P< 0.01; compared with diabetic comparison group, ^#P< 0.05, ^{# #}P< 0.01.

3.1.4 Effects of different intensity aerobic exercise on gastrointestinal motility in diabetic rats

Table 3
Analysis of changes in gastric residual rate and intestinal propulsion rate in rats ( $\bar{r}\pm s$ , $n=$ 6)

Group	Gastric residual rate (%)		Intestinal propulsion rate (%)
N	22	$\pm$ 2.5	50.6	$\pm$ 3.7
D	42	$\pm$ 4.3^∗∗	29.5	$\pm$ 1.8^∗∗
LD	32	$\pm$ 4.2^#	39.8	$\pm$ 5.3^{# #}
MD	29	$\pm$ 3.6^{# #}	41.7	$\pm$ 1.6^{# #}
HD	37	$\pm$ 5.1^{# #}	32.8	$\pm$ 4.2^#

Note: Compared with peaceful comparisonl group, ^**P< 0.01; compared with diabetic comparison group, ^#P< 0.05, ^{# #}P< 0.01.

Following the experiment, Table 3 shows that the intestinal propulsion rate of normal rats was remarkably decreased than that of diabetic rats ( $P<$ 0.05, $P<$ 0.01) and that the gastric residual rate of the rats in each aerobic exercise group was remarkably increased than that of diabetic rats ( $P<$ 0.05, $P<$ 0.01), especially in the middle-intensity group.

3.1.5 Effect of different intensity aerobic exercise on intestinal flora of diabetic rats

Table 4
Changes in intestinal flora of rats in each group ( $\bar{r}\pm s$ , $n=$ 6)

Group	Bacteroides pseudomalli (CFU/g)		Enterobacteriaae (CFU/g)		Bifidobacteria (CFU/g)		Lactobacillus (CFU/g)		Enterococcus (CFU/g)
N	13.2	$\pm$ 3.2	7.2	$\pm$ 2.4	9.5	$\pm$ 2.0	12.3	$\pm$ 2.8	8.3	$\pm$ 0.4
D	8.1	$\pm$ 2.5^∗∗	10.1	$\pm$ 0.4^∗∗	7.3	$\pm$ 0.6^∗∗	7.6	$\pm$ 4.3^∗∗	6.1	$\pm$ 0.2^∗∗
LD	0.9	$\pm$ 2.2^{# #}	9.04	$\pm$ 0.8^#	8.3	$\pm$ 1.3^{# #}	9.4	$\pm$ 1.6^{# #}	7.4	$\pm$ 0.5^{# #}
MD	11.4	$\pm$ 0.9^{# #}	8.27	$\pm$ 1.7^{# #}	8.9	$\pm$ 0.8^{# #}	10.3	$\pm$ 1.7^{# #}	8.0	$\pm$ 1.4^{# #}
HD	9.1	$\pm$ 0.8^#	9.2	$\pm$ 0.3^#	8.1	$\pm$ 0.2^{# #}	8.7	$\pm$ 0.8^#	6.6	$\pm$ 0.1^#

Note: Compared with peaceful comparison group, ^**P< 0.01; compared with diabetic comparison group, ^#P< 0.05, ^##P< 0.01.

Following the experiment, Table 4 shows that the number of enterobacteria in the diabetic rats was remarkably increased than that in the peaceful comparison group after the completion of the experiment, and the number of Bacillus, Bifidobacterium, Lactobacillus and Enterococcus was remarkably decreased ( $P<$ 0.05, $P<$ 0.01); the number of enterobacteria in the rats in each aerobic exercise group was remarkably decreased than that in the diabetic rats, and the number of Bacillus, Bifidobacterium, Lactobacillus and Enterococcus was remarkably increased ( $P<$ 0.05, $P<$ 0.01), especially in the middle-intensity aerobic exercise group, the most significant changes were observed.

3.2 Discussion

There are differences in the influence of different intensities of aerobics on gut flora changes, and research into appropriate exercise loads will provide theoretical support for formulating exercise prescriptions for diabetic.

Diabetes is associated with impaired glucolipid metabolism, and leptin and insulin are involved in glucolipid metabolism [6]. Experimental results show that glucolipid metabolism is impaired in rats with type 2 diabetes; the important role of exercise in improving glucolipid metabolism has been widely confirmed, and aerobic exercise plays an excellent role in promoting lipid metabolism due to its long duration, high total energy expenditure, and high proportion of fat energy supply, while intestinal flora disorders and intestinal inflammatory factors are also closely related to lipid metabolism disorders, and with increasing physical activity, the improvement of lipid metabolism disorder is accompanied by a change in the diversity of intestinal flora and a decrease in intestinal inflammatory response, which not only controls weight but also improves the symptoms of type 2 diabetes. Leptin, a peptide hormone, is involved in energy metabolism, inhibits insulin, and reduces hyperinsulinemia [7]. This study found that in rats with the disease, leptin levels significantly increased. This increase in leptin level suppressed appetite, which in turn affected the digestive system’s ability to function normally. Conversely, insulin levels also significantly increased, but blood glucose levels rose as well, indicating that insulin’s effectiveness was reduced and that blood glucose levels increased. The literature indicates that physical exercise lowers leptin levels and improves its sensitivity, thereby improving leptin resistance [8]. Studies have shown that serum leptin levels decrease after exercise, with the greatest decrease occurring during moderate-intensity aerobic exercise. This could be due to the secretion of leptin from adipose tissue, and when aerobic exercise is continued, fat metabolism accelerates, which inhibits leptin synthesis. The decrease in leptin levels was accompanied by an attenuation of the inhibitory effect on gastrointestinal function, as well as a decrease in insulin levels and blood glucose levels, suggesting increased insulin sensitivity.

The main role of MOT and GAS is to promote and influence gastrointestinal motility [9]. Studies on gastrointestinal hormone secretion and type 2 diabetes are uncommon, despite the literature’s suggestion that the start of type 2 diabetes is more frequently linked to gastrointestinal dysfunction. The results of the current investigation demonstrated that in diabetic rats, gastrointestinal motility problems were linked to gastrointestinal hormone alterations. Following exercise, there were considerable increases in GAS and MOT levels, a notable decrease in residual gastric rate, and a notable rise in intestinal propulsion rate. Exercise appears to improve gastrointestinal issues in type 2 diabetes in conjunction with the levels of GAS and MOT, as the most notable changes were seen in the low-intensity exercise group and the middle-intensity exercise group. In rats with type 2 diabetes, no significant improvement in the tendency toward decreased gastric motility, slowed gastrointestinal motility, and decreased secretion of gastrointestinal hormones was observed with high-intensity exercise. The findings of the experiment point to the impact of exercise on digestive and absorptive functions may be related to the intensity of exercise, which is too high and has an inhibitory effect on the active function of the gastrointestinal tract, while low and moderate intensity exercise causes a positive improvement in the function of the digestive tract and promotes digestion and absorption. The mechanism includes the imbalance of neuro-endocrine immune regulation, endocrine, blood supply of gastrointestinal tract, morphological and structural changes of gastrointestinal mucosa, etc. The possible mechanism needs further investigation.

According to contemporary research, maintaining a balanced condition of intestinal flora is the cornerstone of optimal intestinal function and has emerged as a new goal for the management of several disorders, including diabetes [10]. The results of studies in the literature have demonstrated that the type 2 diabetes is linked to changes in intestinal flora when increased glucose and lipid metabolism is accompanied by a decrease in the number of beneficial bacteria in the gut [11]; following a series of treatments, a decrease in glucose and lipids was found along with an increase in the number of beneficial bacteria, suggesting that changes in intestinal flora are linked with type 2 diabetes [12]. Exercise has been found to enhance intestinal flora both in terms of quantity and composition, preserving an equilibrium that protects the ecological health of the gut, slows metabolic disruptions, and actively fights inflammatory agents. The current study demonstrated that the intestinal flora of rats with type 2 diabetes was disturbed, which is consistent with earlier studies. The increase in blood glucose level in these rats was accompanied by an important increase of bacilli and a significant decrease of helpful bacteria in the intestine. Insulin sensitivity, lipid metabolism, and energy storage are all impacted by intestinal flora abnormalities in type 2 diabetic rats. Disturbances in glucolipid metabolism also play an important role in the onset of diabetes.

Findings from the research revealed that following exercise intervention, particularly the most significant effect of moderate intensity exercise, the number of enterobacteria in the colon greatly dropped and the number of helpful bacteria significantly rose. This shows that aerobic exercise was beneficial in reducing the symptoms of diabetes and that the composition and variety of the gut flora improved to variable degrees following workouts of different intensities. The direct link connecting exercise, intestinal flora, and diabetes is unclear, however this shows that exercise promotes benign changes in intestinal flora as a substitute for treating metabolic illnesses. Studies in the literature have demonstrated that different experimental models have different effects on gut flora and that exercising on a running table differs significantly from exercising on your own [13]. There are differences between the effects of various exercise loads and intensities on the alterations of intestinal flora, as well as between the effects of exercise induction on intestinal flora in various phenotypic animal models. Hence, a stronger theoretical framework for the creation of exercise prescriptions will result from examining the appropriate exercise load amounts in diverse phenotypic models. The symptoms of intestinal flora dysbiosis worsen after intense physical activity, which may be due to increased permeability of the intestine and increased penetration of bacteria from the intestine into the blood, leading to further inflammation, which in turn affects the work of the organism.

4. Conclusion

Type 2 diabetes is a documented metabolic illness, and exercise interventions can successfully halt the onset and progression of the condition. Further research is needed to determine whether exercise can prevent metabolic illnesses by controlling the body’s level of inflammation and the homeostatic balance of the gut flora. Diabetic patients have dysbiosis of intestinal flora, which impacts glucose metabolism through a variety of pathways. The intestinal flora is directly associated to the development of diabetes. Different levels of aerobic exercise have an impact on the changes in intestinal flora, but moderate-intensity exercise has the biggest impact on controlling these changes as well as gastrointestinal hormones, glucose tolerance, insulin resistance, and blood sugar levels. To investigate the potential mechanisms and offer a theoretical framework for the creation of a more powerful exercise regimen for the treatment of diabetes.

Footnotes

Acknowledgments

The National Natural Science Foundation of China (Grant: 3236190210), the Conventional Project of Shaanxi Provincial Sports Bureau (Grant: 2023021), the Conventional Project of Shaanxi Provincial Sports Bureau (Grant: 2023022).

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Effects of different intensity aerobic exercise on intestinal flora and gastrointestinal hormones in type 2 diabetic rats

Abstract

Keywords

1. Introduction

2. Experimental procedure

2.1 Main reagents and instruments

2.2 Experimental animal grouping and the establishment of its diabetes model

2.3 Aerobic exercise program

2.4 General index observation records and sample collection

2.5 Measurement of gastric emptying rate and intestinal propulsion rate

2.6 Biochemical indicators and their determination methods

2.7 Statistical evaluation

3. Results and discussion

3.1 Results

3.1.1 General situation analysis in rats of each group

3.1.2 Comparative analysis of changes in serum levels of GAS, MOT, and leptin in rats of each group

Table 1 Changes of GAS, MOT and Leptin levels in the serum of rats ( r ¯ ± s , n = 6)

Table 2 Analysis of changes in blood glucose and lipid levels in rat serum ( r ¯ ± s , n = 6)

Table 3 Analysis of changes in gastric residual rate and intestinal propulsion rate in rats ( r ¯ ± s , n = 6)

Table 4 Changes in intestinal flora of rats in each group ( r ¯ ± s , n = 6)

4. Conclusion

Footnotes

Acknowledgments

References

Table 1
Changes of GAS, MOT and Leptin levels in the serum of rats ( $\bar{r}\pm s$ , $n=$ 6)

Table 2
Analysis of changes in blood glucose and lipid levels in rat serum ( $\bar{r}\pm s$ , $n=$ 6)

Table 3
Analysis of changes in gastric residual rate and intestinal propulsion rate in rats ( $\bar{r}\pm s$ , $n=$ 6)

Table 4
Changes in intestinal flora of rats in each group ( $\bar{r}\pm s$ , $n=$ 6)