The Effect of Swimming Training at Different Temperatures with Cinnamon Consumption on Avoidance Memory and Aerobic Power in Streptozotocin- Induced Diabetic Rats

Subject Areas : Open Access

Omidreza Salehi ¹ , Dariush Sheikholeslami -Vatani ² , Zahra Negarandeh ³ , Jalal Yarahmadi ⁴

1 - Department of Physical Education and Sport Sciences, University of Kurdistan, Sanandaj, Iran
2 - Department of Physical Education and Sport Sciences, University of Kurdistan, Sanandaj, Iran
3 - Nutrition Research Center, Shiraz University of Medical Sciences, Shiraz, Iran
4 - Department of Physical Education and Sport Sciences, Payame Noor University, Iran

Received: 2020-12-19 Accepted : 2020-12-19 Published : 2020-11-21

Keywords: Cinnamon, Diabetes mellitus, Aerobic power, swimming training, Avoidance Memory,

Abstract :

Abstract Introduction: Diabetes is a metabolic disease that causes cognitive disorders in addition to physical injuries. The role of physical activity and medical plants in improving memory and physical function has been reported, but the interactive effect of training at different temperatures with Cinnamon consumption has not been known yet. Therefore, the present study aimed to investigate the effect of swimming (S) training in water at 5 ° C (S5C) and 35 ° C (S35C) with cinnamon (Cin) consumption on avoidance memory, spatial memory and aerobic power of diabetic rats. Material and methods: In this experimental study, 48 diabetic rats (55 mg/kg streptozotocin) were divided into 1) diabetic control (CD), 2) S5C, 3) S5C+Cin, 4) S35C, 5) S35C+Cin and 6) Cin groups. Eight rats were placed in the healthy control (HC) group to investigate the effects of diabetes induction on the research variables. Swimming trainings were performed at 2±5 ° C and 36±2 ° C for eight weeks, 3 days per week and 2-4 minutes in each session. The aqueous extract of cinnamon was 200 mg/kg/day dissolved in drinking water. 48 hours after the last training session, the research variables were measured. Findings: S5C and S35C significantly caused the increase in step through latency (STL), percentage of alteration (PA) and aerobic power as well as decreased time spent in dark compartment (TDC) and repeat dark entrances (RDE) (P≤0.05). Cin caused a significant increase in PA and aerobic power as well as significant decrease in TDC (P≥0.05). Also, S5C+Cin and S35C+Cin significantly increased STL and PA and decreased TDC in diabetic rats (P≥0.05). Conclusion: It seems that swimming training at different temperatures and consuming cinnamon have beneficial effects on the memory and learning of diabetic rats, but since Cin moderated the effects of training, further studies at the molecular- cellular level are recommended. Keywords: Training, Cinnamon, Memory, Aerobic Power, Diabetes   Extended abstract Introduction Diabetes mellitus is characterized by abnormal metabolism, decreased insulin secretion, increased insulin resistance, or both (1). This disease is associated with decreased levels of neurotrophins, increased inflammatory factors in the central nervous system following increased oxidative stress (3, 4). Decreased neuroplasticity and neurotrophins are associated with cognitive impairment, decreased balance, decreased aerobic power, and decreased quality of life (5). But exercises improve neurotrophins and memory, increase neuroplasticity and reduce anxiety as well as depression (8). Cinnamon (Cin) also improves memory and learning in Alzheimer's patients with its antioxidant, anti-inflammatory, amyloid-beta-reducing effects and improved cerebral circulation (13). In addition, cold pressure has beneficial effects on reducing white adipose tissue and increasing brown adipose tissue (11); however, studies on the effect of training at different temperatures along with Cin on cognitive function are limited. Therefore, the present study aimed to investigate the effect of eight weeks of swimming training at different temperatures along with Cin on the avoidance memory, spatial memory and aerobic power of streptozotocin- induced diabetic rats.   Materials and methods In this experimental study, 48 diabetic rats (55 mg/kg streptozotocin peritoneal injected manufactured by Sigma USA) based on fasting blood glucose divided into1) diabetic control (CD), 2) swimming training in temperatures of 5 ° C (S5C), 3) S5C+Cin, 4) swimming training in temperature 36 ° C (S35C), 5) S35C+Cin, and 6) Cin groups. Also, eight rats were placed in the healthy control (HC) group to investigate the effects of diabetes induction on the research variables. Swimming trainings were performed at 2±5 ° C and 36±2 ° C. Swimming training protocol was five sessions in each week. Each session lasted 2 minutes for the first week. So 30 seconds were added to the training until the training reaches 4 minutes. By the end of the eighth week, the rats trained for 4 minutes at 5 ° C (16, 17). Also, 200 mg/kg of cinnamon (aqueous extract) was added daily to the drinking water of rats (18). The aqueous extract of cinnamon was 200 mg/kg/day dissolved in drinking water.   Avoidance memory This test was performed 48 hours after the last training session for two days in two consecutive stages. Habituation session, memory acquisition education and memory recovery test were done in three stages based on the study of Zavvari et al. In the memory recovery phase, the rat was placed in a light chamber, and after 20 seconds, the door was opened. The latency which the animal entered the dark chamber (STL), the time spent in the dark chamber (TDC) and the number of repeat dark entrances (RDE) was recorded for each rat during the test period. The test duration was five minutes (19).   Spatial memory This test was performed for 8 minutes using a Y maze in which repeated behaviors were considered as successful and serial entries into all arms in 3 overlapping sets. Thus, the percentage of alteration (PA) was calculated as the maximum alteration (total number of entered arms) multiplied by 100 (19).   Aerobic power To measure the aerobic power, rats warmed up on treadmill for 5 minutes at a speed of 6 m/min with zero-degree incline; then the speed increased 3 m/min every 3 minutes until the rats became exhausted and were no longer able to continue. The criterion for reaching VO2max was the inability of rats to continue the training protocol and three consecutive collisions (three times in a period of 1 minute) with the end of the treadmill (20).   Statistical analysis The normal distribution of findings was investigated using Shapiro- Wilk test and statistical analysis was performed using independent sample t- test, two-way ANOVA with Bonferroni’s post- hoc test in SPSS software version 22 (P≤0.05).   Findings The results of independent sample t- test showed that STL (P=0.001), PA (P=0.001) and VO2max (P=0.001) in HC group were significantly higher than CD group; there was no significant difference in TDC between HC and CD groups (P≥0.05) but RDE in CD group was significantly higher than HC group (P≤0.05). The results of two- way ANOVA test showed that Cin had no significant effect on STL (P=0.85), but S (P=0.001), and interaction of S and Cin significantly increased STL (P=0.04). The results of Bonferroni’s post- hoc test showed that S6C (P=0.001) and S35C (P=0.001) significantly increased STL and there was no significant difference between S6C and S35C (P=0.99). Cin (P=0.01) and S (P=0.001) significantly decreased TDC; moreover, interaction of S and Cin decreased TDC (P=0.03); also, S6C (P=0.02) and S35C (P=0.001) significantly increased TDC and no significant difference was seen between S6C and S35C (P=0.26). Furthermore, Cin (P=0.11) and interaction of S and Cin (P=0.07) had no significant effect on RDE, though, S alone significantly decreased RDE (P=0.002), S6C (P=0.03) and (P=0.002) significantly increased RDE. Also significant difference was not shown between S6C and S35C (P=0.63). In addition, Cin (P=0.001) and S (P=0.001) significantly increased PA, and interaction of S and Cin decreased PA (P=0.001); S6C (P=0.001) and S35C (P=0.001) significantly increased PA and PA levels in S35C group were significantly higher than those of S6C group (P=0.001). Finally, Cin (P=0.02) and S (P=0.001) significantly increased VO2max, but interaction of S and Cin on increase of VO2max was not significant (P=0.67); S6C (P=0.001) and S35C (P=0.001) significantly increased VO2max and no significant difference was seen between S6C and S35C (P=0.99).   Discussion The results showed that S5C and S35C improved avoidance memory, spatial memory and aerobic power in diabetic rats. Diabetes increases amyloid levels in neurons of the nervous system by increasing oxidative stress, inflammatory factors, and mitochondrial defects, and also decreases memory and learning by decreasing neuroplasticity (21). However, physical activity and post-exercise cold pressure by cAMP/PKA/NRF1,2 mechanism and increased PGC-1α increases the expression of uncoupling protein 4 (UCP4) and improves neurotrophins (23). Increased lipid metabolism, increased mitochondrial biogenesis and thermogenesis following exercise in hot and cold weather increase aerobic power (22). Cin also increased PA and VO2max and decreased TDC in diabetic rats. Cin can improve lipid metabolism by antioxidant effects, increase cerebral blood flow, phosphorylation of transcription proteins from metabolic genes, and decrease amyloid levels and has an important role in improving neurotrophins, memory and learning (25). Also, Cin through cAMP/PKA/NRF1,2 pathway and through an increase in mitochondrial biogenesis can improve lipid, glucose and insulin metabolism which ultimately leads to improved aerobic power (26). The results showed that the interaction of S5C+Cin and S35C+Cin increased STL and PA and decreased TDC in diabetic rats. There are limited studies on the simultaneous effect of training and consumption of cinnamon on memory and learning, but training in hot and cold weather from cAMP/PKA/NRF1,2, PGC-1α and UCP4 can improve memory (23) and by improving lipids metabolism, mitochondrial biogenesis and thermogenesis can increase aerobic power (22). Cin also promotes memory and learning through its antioxidant mechanism, increases cerebral blood flow, decreases amyloid beta levels, and improves neurotrophins (25) and the interaction between training and Cin increases aerobic power (26). Not being able to measure the neurotrophins in the nervous system and mitochondrial biogenesis factors are the limitations of this study, so conducting such studies in the future is recommended to researchers.   Conclusion The interaction of S5C + Cin and S35C + Cin seems to have beneficial effects on the memory and learning of diabetic rats, however, since cinnamon modulated the effects of training, further studies at the molecular- cellular level are recommended.   Ethical Considerations Compliance with ethical guidelines The present study was conducted based on the animal ethical guidelines.   Funding No funding.   Authors' contributions Design and conceptualization: Omidreza Salehi, Daryosh Sheikholeslami Vatani; Methodology and data analysis: Omidreza Salehi, Zahra Negarandeh, Jalal Yarahmadi; Supervision and final writing: Daryosh Sheikholeslami Vatani.   Conflicts of interest The authors declared no conflict of interest.

References:

1. Hosseini SA, Hamzavi K, Safarzadeh H, Salehi O. Interactive effect of swimming training and fenugreek (Trigonella foenum graecum L.) extract on glycemic indices and lipid profile in diabetic rats. Arch Physiol Biochem. 2020; 5; 1- 5. [DOI:10.1080/13813455.2020.1826529] [PMID:33017260]


2. Stanciu GD, Bild V, Ababei DC, Rusu RN, Cobzaru A, Paduraru L, et al. Link between diabetes and Alzheimer’s disease due to the shared amyloid aggregation and deposition involving both neurodegenerative changes and neurovascular damages. J Clin Med. 2020; 9 (6): 1713. [DOI:10.3390/jcm9061713] [PMCID:PMC7357086]  


3. Rozanska O, Uruska A, Zozulinska-Ziolkiewicz D. Brain- derived neurotrophic factor and diabetes. Int J Mol Sci. 2020; 21 (3): 841. [DOI:10.3390/ijms21030841] [PMID:32012942]


4. Salehi OR, Hosseini SA, Farkhaie F, Farzanegi P, Zar A. The effect of moderate intensity endurance training with genistein on brain- derived neurotrophic factor and tumor necrosis factor- α in diabetic rats. J Nutr Fasting Heal. 2019; 7 (1): 44– 51. [DOI:10.22038/JNFH.2019.37231.1163]


5. Hosseini SA, Salehi OR, Farzanegi P, Farkhaie F, Darvishpour AR, Roozegar S. Interactive effects of endurance training and royal jelly consumption on motor balance and pain threshold in animal model of the Alzheimer disease. Arch Neurosci. 2020; 7 (2): e91857 [DOI:10.5812/ans.91857]


6. Hansen D, De Strijcker D, Calders P. Impact of endurance exercise training in the fasted state on muscle biochemistry and metabolism in healthy subjects: can these effects be of particular clinical benefit to type 2 diabetes mellitus and insulin-resistant patients?. Sport Med. 2017; 47 (3): 415– 28. [DOI:10.1007/s40279-016-0594-x] [PMID:27459862]


7. Borror A, Zieff G, Battaglini C, Stoner L. The effects of postprandial exercise on glucose control in individuals with type 2 diabetes: a systematic review. Sport Med. 2018; 48 (6): 1479- 91. [DOI:10.1007/s40279-018-0864-x] [PMID:29396781]


8. Negarandeh Z, Mohamadzadeh Salamat K, Hosseini SA, Etemad Z. The effect of endurance training with crocin consumption on IGF-1 and glycogen expression in rat hippocampus tissue of trimethyltin-treated model of Alzheimer’s disease. Asian J Sports Med. 2019; 10 (3): e92246. [DOI:10.5812/asjsm.92246]


9. Salehi OR, Hoseini A. The effects of endurance trainings on serum BDNF and insulin levels in streptozotocin-induced diabetic rats. Shefaye Khatam. 2017; 5 (2): 52– 61. http://shefayekhatam.ir/article-1-1378-en.html


10. Zhao RR, O’Sullivan AJ, Singh MAF. Exercise or physical activity and cognitive function in adults with type 2 diabetes, insulin resistance or impaired glucose tolerance: a systematic review. Eur Rev Aging Phys Act. 2018; 15 (1): 1. [DOI:10.1186/s11556-018-0190-1] [PMCID:PMC5776769]


11. Bukowiecki LJ. Energy balance and diabetes. The effects of cold exposure, exercise training, and diet composition on glucose tolerance and glucose metabolism in rat peripheral tissues. Can J Physiol Pharmacol. 1989; 67 (4): 382- 93. [DOI:10.1139/y89-062] [PMID:2667731]


12. Hanssen MJW, Hoeks J, Brans B, Van Der Lans AAJJ, Schaart G, Van Den Driessche JJ, et al. Short-term cold acclimation improves insulin sensitivity in patients with type 2 diabetes mellitus. Nat Med. 2015; 21 (8): 863. [DOI:10.1038/nm.3891] [PMID:26147760]


13. Anderson RA, Qin B, Canini F, Poulet L, Roussel AM. Cinnamon counteracts the negative effects of a high fat/high fructose diet on behavior, brain insulin signaling and Alzheimer-associated changes. PLoS One. 2013; 8 (12): e83243. [DOI:10.1371/journal.pone.0083243]  [PMCID:PMC3862724]


14. Edalatmanesh MA, Khodabandeh H, Yazdani N, Rafiei S. Effect of cinnamomum zeylanicum extract on memory and hippocampal cell density in animal model of diabetes. J Arak Univ Med Sci. 2018; 21 (6): 56– 66. http://jams.arakmu.ac.ir/article-1-5738-en.html


15. Momtaz S, Hassani S, Khan F, Ziaee M, Abdollahi M. Cinnamon, a promising prospect towards Alzheimer’s disease. Pharmacol Res. 2018; 130: 241– 58. [DOI:10.1016/j.phrs.2017.12.011]  [PMID:29258915]


16. Lubkowska A, Bryczkowska I, Gutowska I, Rotter I, Marczuk N, Baranowska-Bosiacka I, et al. The effects of swimming training in cold water on antioxidant enzyme activity and lipid peroxidation in erythrocytes of male and female aged rats. Int J Environ Res Public Health. 2019; 16 (4): 647. [DOI:10.3390/ijerph16040647] [PMCID:PMC6406484]


17. Bryczkowska I, Baranowska-Bosiacka I, Lubkowska A. Effect of repeated cold water swimming exercise on adaptive changes in body weight in older rats. Cent Eur J Sport Sci Med. 2017; 18 (2): 77- 87. [DOI:10.18276/cej.2017.2-08]


18. Ismail NS. Protective effects of aqueous extracts of cinnamon and ginger herbs against obesity and diabetes in obese diabetic rat. World J Dairy Food Sci. 2014; 9 (2): 145- 53. [DOI:10.5829/idosi.wjdfs.2014.9.2.1137]


19. Zavvari F, Karimzadeh F. A review on the behavioral tests for learning and memory assessments in rat. Neurosci J Shefaye Khatam. 2017; 5 (4): 110- 24. http://shefayekhatam.ir/article-1-1419-fa.html


20. Li FH, Sun L, Zhu M, Li T, Gao H-E, Wu D-S, et al. Beneficial alterations in body composition, physical performance, oxidative stress, inflammatory markers, and adipocytokines induced by long-term high-intensity interval training in an aged rat model. Exp Gerontol. 2018; 113: 150–62. [DOI:10.1016/j.exger.2018.10.006] [PMID:30308288]


21. Sun Y, Ma C, Sun H, Wang H, Peng W, Zhou Z, et al. Metabolism: A novel shared link between diabetes mellitus and Alzheimer’s disease.J Diabetes Res. 2020; 29: 4981814. [DOI:10.1155/2020/4981814] [PMID:32083135]


22. Ihsan M, Watson G, Abbiss CR. PGC-1α mediated muscle aerobic adaptations to exercise, heat and cold exposure. J Cell Mol Exer Physiol. 2014; 3(1):e7. http://www.cellularandmolecularexercisephysiology.com/index.php/CMEP/article/view/e7/


23. Tsai Y-J, Jhong Y-C, Ching S-H, Liao Y-C, Ching C-H, Chuang J-I. Cold exposure after exercise impedes the neuroprotective effects of exercise on thermoregulation and UCP4 expression in an MPTP- induced Parkinsonian mouse model. Front Neurosci. 2020; 14: 944. [DOI:10.3389/fnins.2020.573509] [PMCID:PMC7522410]


24. Yang L, Wu J, Hu Z, Gao F, Hu X. Effects of workload on human cognitive performance of exposure to extremely cold environment. Physiol Behav. 2020; 113296. [DOI:10.1016/j.physbeh.2020.113296]


25. Frydman-Marom A, Levin A, Farfara D, Benromano T, Scherzer-Attali R, Peled S, et al. Orally administrated cinnamon extract reduces β-amyloid oligomerization and corrects cognitive impairment in Alzheimer’s disease animal models. PLoS One. 2011; 6 (1): e16564. [DOI:10.1371/journal.pone.0016564] [PMCID:PMC3030596]


26. Rahmat M, Kazemi A, Kerendi H, Sheibak A. The effect of HIIT with supplementation of cinnamon on DPP4 concentration, insulin resistance, BMI and Vo_2max in overweight boys. J Appl Exer Physiol. 2019; 15 (19): 119- 132. [DOI:10.22080/JAEP.2019.14871.1801]


27. Yulug B, Cankaya S. Translational perspective: is cinnamon a suitable agent for cognitive impairment and Alzheimer’s disease associated with brain trauma?. Neural Regen Res. 2019; 14 (8): 1372. [DOI:10.4103/1673-5374.253518] [PMCID:PMC6524496]