The Effect of Four Weeks of Lemon Essential Oil Consumption and Swimming Training on Memory and Pain in Adult Male Mice
Subject Areas : Journal of Animal Biology
Sara
Ahmadizadeh
1
(Department of Physical Education and Sport Sciences, Ahvaz Branch, Islamic Azad University, Ahvaz, Iran)
Abdolhassan
Doulah
2
(Department of Biology, Ahvaz Branch, Islamic Azad University, Ahvaz, Iran)
Maryam
Rafieirad
3
(Department of Biology, Izeh Branch, Islamic Azad University, Izeh, Iran)
Keywords: pain, Memory, swimming training, Lemon essential oil, Adult male mice,
Abstract :
With age, some functions of the nervous system, including avoidance memory, are impaired. The beneficial effects of exercise on neurogenesis, increasing neuronal synapses, the treatment of mental disorders, helping improve brain injuries, and prevention of neurodegenerative diseases have been proven. Citrus limon is one of the plants mentioned in traditional medicine for its analgesic effects. Therefore, in the present study, the effect of four weeks of lemon essential oil consumption and swimming training on memory and pain in male mice was investigated. To this end, 40 male mice with a weight of 40± 5 g were studied. The mice were randomly divided into 4 groups including control, swimming group, group receiving lemon essential oil, and group of swimming training + consuming lemon essential oil. Swimming practice consisted of four weeks of swimming in water for 30 minutes per session and five sessions per week, and 50 mg/kg lemon essential oil was administered by gavage. The pain threshold was measured to evaluate the avoidance memory of the shuttle box using the tail flick test. The results showed that the essential oil of lemon and swimming training has significantly reduced pain (p < 0.001). Moreover, the combined consumption of lemon essential oil and swimming training increased memory in male mice (p < 0.001). Aerobic exercise, especially swimming, has had a positive effect on memory consolidation and reduction of pain threshold. Probably, consuming lemon essential oil due to the presence of strong antioxidants can reduce the feeling of pain and improve avoidance memory.
1. Aguiar Jr A.S. 2010. High-intensity physical exercise disrupts implicit memory in mice: involvement of the striatal glutathione antioxidant system and intracellular signaling. Neuroscience, 171(4): 1216-1227.
2. Amaral JF., Silva MIJ., Neto MRA., Neto PFT., Moura BA., Melo C.T.V. 2007. Antinociceptive effect of the monoterpene R(+) Limonene in Mice. Biology and Pharmacology Bulletin, 30(7): 1217-1220.
3. Amin G.R. 1991. Popular medicinal plants of Iran. Iranian Research Institute of Medicinal Plants, Tehran, 1-66. (In Persian)
4. Amorim J.L., Simas D.L.R., Pinherio M.G., Moreno D.A., Alviano C.S., Silva A.R. 2016. Anti-inflammatory properties and chemical characterization of the essential oils of four citrus species. Plos One, 11(4): 1-18.
5. Ang E.T., Dawe G.S., Wong P.T.H., Moochhala S., Ng Y.K. 2013. Alterations in spatial learning and memory after forced exercise. Brain Research, (1):186-193.
6. Archer T. 2012. Influence of physical exercise on traumatic brain injury deficits: Scaffolding effect. Neurotoxological Research, 21: 418-434.
7. Balsinde J., Balboa M.A., Dennis E.A. 2000. Group IV cytosolic phospholipase A2 activation by diacylglycerol pyrophosphate in murine P388D1 macrophages. Annals of the New York Academy ofSciences, 905(1): 11-15.
8. Boudouda H.B., Zeghib A., Karioti A., Bilia A.R., Oztürk M., Aouni M., et al. 2015. Antibacterial, antioxidant, anti-cholinesterase potential and flavonol glycosides of Biscutella raphanifolia (Brassicaceae). Pak J Pharm Sci. 28(1): 153-158.
9. Campelo L.M.L., Almeida A.A.C., Freitas R.L.M., Ceraqueira G.S., Sousa G.F., Saldanha G.B. 2011. Antioxidant and antinociceptive effects of citrus limon essential oil in mice. Journal of Biomedicine and Biotechnology, (1): 1-8.
10. Carrera-Quintanar L., Funes L., Viudes E., Tur J., Micol V., Roche E. 2012. Antioxidant effect of lemon verbena extracts in lymphocytes of university students performing aerobic training program. Scandinavian Journal of Medical Science and Sports, 22(4): 454-461.
11. Chaddock, L.2011. A review of the relation of aerobic fitness and physical activity to brain structure and function in children. Journal of the International Neuropsychological Society, 17(06): 975-985.
12. Davoodian-Dehkordi A., Hojjati M., Yousefi M., Moshtaghi A., Rahimian R., Rafieian M. 2011. The effect of hydro-alcoholic extract of dried Ficus carica on spatial learning and memory in mice. Journal of Shahrekord University Medical Sciences, 12(4): 1-7.
13. Eidi M, Eidi A, Bahar M. 2006. Effects of Salvia officinalis L. (sage) leaves on memory retention and its interaction with the cholinergic system in rats. Nutrition, 22(3): 321-326.
14. Garcia P.C. 2012. Different protocols of physical exercise produce different effects on synaptic and structural proteins in motor areas of the rat brain. Brain Research, 1456(0): 36-48.
15. Gholamrezaei S., Taati M. 2016. Interaction between melatonin and exercise in the spatial memory and learning performance in rats. Scientific Journal of Kurdistan University, 21(2):75-84.
16. Gobeske K.T., Das S., Bonaguidi M.A., Weiss C., Radulovic J., Disterhoft J.F. 2009. BMP signaling mediates effects of exercise on hippocampal neurogenesis and cognition in mice. PLoS One, 4(10): e7506-7507.
17. Gomes P., Oliveira H., Vicente A., Ferreira M. 2006. Production, transformation and essential oils composition of leaves and stems of lemon verbena Aloysia triphylla (L’Herit.) Britton grown in Portugal. Review in Brazilian Plant Medicine, 8:130-135.
18. Gomes da Silva S.2012. Early exercise promotes positive hippocampal plasticity and improves spatial memory in the adult life of rats. Hippocampus, 22(2): 347-358.
19. Hajisoltani R., Rashidy-Pour A., Vafaei, A.A., Ghaderdoost B., Bandegi A.R., Motamedi F. 2011. The glucocorticoid system is required for the voluntary exercise-induced enhancement of learning and memory in rats. Behavior and Brain Research, 219: 75-81.
20. Hayden J.A., Van Tulder. M.W., Malmivaara A.V., Koes BW. 2005. Metaanalysis: Exercise therapy for nonspecific low back pain. Annual of Internal Medicine, 142: 765-75.
21. Hejazian E., Sadeghian, M., Hejazian, S.2016.The Role of Aerobic Exercise on Pain By Histamine Receptors Using Formalin Test in Mice. Journal of Rafsanjan University Medical Sciences, 15(1):17-26.
22. Hoveida R., Alaei H., Oryan S., Parivar K., Reisi P.2011. Treadmill running improves spatial memory in an animal model of Alzheimer's disease. Behavior and Brain Research, 216: 270-274.
23. Hubert M.2011. Physical therapy for Parkinson’s disease. Revue Medicale de Bruxelles, 32: 388-392.
24. Kamrani F., Nazari M., Sahebalzamani M., Amin G., Farajzadeh M.2016. Effect of Aromatherapy With Lemon Essential Oil on Anxiety after Orthopedic Surgery, IJRN; 2(4): 26-31.
25. Katsuyama S., Otowa A., Kamio S., Sato K., Yagi T., Kishikawa Y. 2015. Effect of plantar subcutaneous administration of bergamot essential oil and linalool on formalin induced nociceptive behavior in mice. Biomedical Research, 36(1): 47-54.
26. Kimani S.T., Nyongesa A.W. 2008. Effects of single daily khat (Catha edulis) extract on spatial learning and memory in CBA mice. Behavior and Brain Research, 195(1): 192-197.
27. Khalil Z., Liu T., Helwe R.D. 1999. Free radicals contribute to the reduction in peripheral vascular responses and the maintenance of thermal hyperalgesia in rats with chronic constriction injury. Pain, 79(1): 31-37.
28. Kummer R., Fachini-Queiroz F.C., Estevao-Silva C.F., Grespan R., Leite Silva E., Bersani-Amado C.A. 2013. Evaluation of anti-inflammatory activity of Citrus latifolia tanaka essential oil and limonene in experimental mouse models. Evidence-Based Complementary and Alternative Medicine, 2013(2): 1-8.
29. Kuphal K.E., Fibuch E.E., Taylor B.K. 2007. Extended swimming exercise reduces inflammatory and peripheral neurophatic pain in rodents. Journal of Pain, 8: 989-997.
30. Knochel C., Oertel-Knochel V., O’Dwyer L., Prvulovic D., Alves G., Kollmann B. 2012. Cognitive and behavioral effects of physical exercise in psychiatric patients. Progressive Neurobiology, 96: 46-68.
31. Kohler CA., daSilva W.C., Benetti F., Bonini J.S. 2011. Histaminergic mechanisms for modulation of memory systems. Neural Plast, 32: 1-16.
32. Ikeda H., Takasu S., Murase K. 2014. Contribution of anterior cingulate cortex and descending pain inhibitory system to analgesic effect of lemon odor in mice. Molecular Pain, 10(14): 1-8.
33. Larson E.B., Wang L., Bowen J.D. McCormick W.C., Teri L., Crane P., Kukull W. 2006. Exercise is associated with reduced risk for incident dementia among persons 65 years of age and older. Annals of Internal Medicine, 144: 73-81.
34. Li H., Liang A., Guan F., Fan R., Chi L., Yang B. 2013. Regular treadmill running improves spatial learning and memory performance in young mice through increased hippocampal neurogenesis and decreased stress. Brain Research, 1531: 1-8.
35. Lin T.W. 2012. Different types of exercise induce differential effects on neuronal adaptations and memory performance. Neurobiology of Learning and Memory, 97(1): 140-147.
36. Liu Y.F., Chen H.I., Wu C.L., Kuo Y.M., Yu L., Huang AM., Wu FS., Chuang J.I., Jen C.H. J. 2009. Differential effects of treadmill running and wheel running on spatial or aversive learning and memory: roles of amygdalar brain-derived neurotrophic factor and synaptotagmin I. The Journal of Physiology, 587(13): 3221-3231.
37. Mahmoudi R., Rafieirad M., Goudarzi S. 2018. Effect of hydroalcoholic extract of Ferulago angulata (Schlecht) boiss on motor and memory disorders in animal model of parkinson disease. Qom University of Medical Science Journal, 12(8): 36-47.
38. Marlatt M.W., Potter M.C., Lucassen P.J., van Praag H. 2012. Running throughout middle age improves memory function, hippocampal neurogenesis, and BDNF levels in female C57BL/6J mice. Developmental Neurobiology, 72: 943-52.
39. Mazzardo-Martins L., Martins D.F., Marcon R., Dos Santos U.D., Speckhann B., Gadotti V.M. 2010. High-intensity extended swimming exercise reduces pain-related behavior in mice: involvement of endogenous opioids and the serotonergic system. Journal of Pain, 11(12): 1384-1393.
40. Mirzapour S., Rafieirad M., Rouhi L. 2015. Hydroalcoholic extract of ferulago angulata improves memory and pain in brain hypoperfusion ischemia in rats. Jundishapur Journal of Natural Pharmacology Prod, 10(1): e17451.
41. Mohammadifar M., Tamtaji O.R., Behnam M., Taghizadeh M., Talae S.A. 2016. Analgesic effect of alcoholic extract of Morus alba L. leaf on male rats. Horizon of Medical Sciences, 22(2): 151-158.
42. Mojtahedin A. 2016. Investigation of Peripheral Effects of Citrus Limon Essential Oil on Somatic Pain in Male Wistar Rats: Role of Histaminergic System. Journal of Fasa University of Medical Sciences, 6: 399-408.
43. Mokhtari M., Shariati M., Sadeghi N. 2008. Effect of alcohol extract from leave Juglans regia on antinociceptive induced by morphine in formalin test. Medical Sciences, 18(2): 85-90.
44. Navarra M., Mannucci C., Delbo M., Calapai G.2015. Citrus bergamia essential oil: from basic research to clinical application. Frontiers in Pharmacology, 6(36): 1-7.
45. Ogeturk M., Kose E., Sarsilmaz M. 2010. Effects of lemon essential oil aroma on the learning behaviors of rats. Neurosciences, 15(4): 292-3.
46. Passos F.B., Lopes E.M., Araujo J.M., Sousa D.P., Veras L.M., Leite J.R. 2015. Involvement of cholinergic and opioid system in γ terpinenemediated anti niciception. Evidence Based Complementary and Alternative Medicine, 20(1): 1-10.
47. Pergolizzi J., Böger RH., Budd K., Dahan A., Erdine S., Hans G. 2008. Opioids and the management of chronic severe pain in the elderly: consensus statement of an international expert panel with focus on the six clinically most often used World Health Organization step III opioids (buprenorphine, fentanyl, hydromorphone, methadone, morphine, oxycodone). Pain Practice, 8(4): 287-313.
48. Picq M., Cheav SL., Prigent A.F. 1991. Effect of two flavonoid compounds on central nervous system. Analgesic activity. Life Science, 49(26): 1979-88.
49. Purves D., Augustine GJ., Fitzpatrick D., Hall WC., LaMantia AS., McNamara JO. 2008. Neuroscience, 4th ed. Masachusetts: Sinauer Associates Inc, pp: 799-804.
50. Quintans Junior L.J., Guimaraes A.G., Santana M.T., Araujo B.E., Moreira F.V., Bonjardim LR. 2011. Citral reduces nociceptive and inflammatory response in rodents. Brazilian Journal of Pharmacology, 21(3): 497-502.
51. Rabiei Z., Hojjati M., Moradi- Nafchi A., afieian-kopaei M. 2015. Effect of various doses of Lavandula officinalis on acute pain in rat. Razi Journal of Medical Sciences, 22(135): 115-121.
52. Rafiei F., Ramezani R. 2012. Antimicrobial effects of lemon essential oil and extract (juice) on oral microorganisms. Scientific-Research Journal of Microbial Biotechnology, 14(4): 1-7.
53. Robb K.A., Williams J.E., Duvivier V., Newham, D.J. 2006. A pain management program for chronic cancertreatment- related pain: A preliminary study. Pain, 7: 82-90.
54. Saadati, H. 2010. Effects of exercise on memory consolidation and retrieval of passive avoidance learning in young male rats. Asian Journal of Sports Medicine, 1(3): 137-142.
55. Samsamshariat SH., Moattar F. 2004. Treatment with plant. 9th ed. Tehran: Roozbahan Publication, 13-17.
56. Shirzad H., Shahrani M., Rafieian-Kopaei M. 2009. Comparison of morphine and tramadol effects on phagocytic activity of mice peritoneal phagocytes in vivo. International Immunopharmacology, 9(7-8): 968-970.
57. Taati M., Moghaddasi M., Eesmaeili M., Pourkhodadadd S., HassanNayebzadeh H. 2014. The role of the central histaminergic receptors in the exercise-induced improvements of the spatial learning and memory in rats. Brain Research, 1587: 112-118.
58. Taherian A., Rashidy-Pour A., Vafaei A., Jarrahi M., Miladi-Gorgi H., Emami-Abarghooii M. 2004. Effect of aqueous extract of the Coriandrum sativum seed on the reduction of acute and chronic pain in mice. Journal of Rafsanjan University Medical Sciences, 3(4): 243-249.
59. Tomotake H., Koga T., Yamato M., Kassu A., Ota F. 2006. Antibacterial activity of Citrus fruit juices against vibrio species. Journal of Nutrition Science and Vitaminology, 52(2): 157-160.
60. Tsujiyama I., Mubassara S., Aoshima H., Hossain S.J. 2013. Antihistamine release and anti-inflammatory activities of aqueous extracts of citrus fruits peels. Oriental Pharmacology and Experimental Medicine, 13(3): 175-180.
61. Vaynman S., Ying Z., Gomez-Pinilla F. 2004. Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. European Journal of Neurosciences, 20: 2580-2590.
62. Veisi M., Shahidi S., Komaki A., Sarihi A. 2014. Effect of Lemon Verbena on Memory of Male Rats.Avicenna Journal of Neuropsycho Physiology, 1(2): 69-72.
63. Viuda-Martos M., Ruiz-Navajas Y., Fernandez-Lopez J., Perez-Alvarez J. 2008. Antifungal activity of lemon (Citrus lemon L.), mandarin (Citrus reticulata L.). Arts Research Journal, 3(4): 141.
64. Vollala V.R., Upadhya S., Nayak S. 2010. Effect of Bacopa monniera Linn. (brahmi) extract on learning and memory in rats: A behavioral study. Journal of Veterinary Behavior: Clinical Applied Research, 5(2): 69-74.
65. Williams C.M., El Mohsen M.A., Vauzour D., Rendeiro C., Butler LT., Ellis JA. 2008. Blueberry-induced changes in spatial working memory correlate with changes in hippocampal CREB phosphorylation and brain-derived neurotrophic factor (BDNF) levels. Free Radical Biology and Medicine, 45(3): 295-305.
66. Zar A., Hoseini A., Ahmadi F., Rezaei M. 2016. Effects of ginger together with swimming training on blood fat profiles in adult diabetic rats with streptozotocin. Iranian Journal of Nutrition Sciences and Food Technology, 11(2): 65-74.
67. Zargari A. 1997. Medicinal plants. 7th ed. Tehran: Tehran University Publication, pp: 488-495.
_||_