Login Register Cart 0
Generic placeholder image

CNS & Neurological Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5273
ISSN (Online): 1996-3181

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
General Research Article

The Protective Effects of the Combination of Vitamin E and Swimming Exercise on Memory Impairment Induced by Exposure to Waterpipe Smoke

Author(s): Karem H. Alzoubi*, Abdulsalam M. Halboup, Omar F. Khabour and Mahmoud A. Alomari ⁠

Volume 22, Issue 2, 2023

Published on: 23 May, 2022

Page: [304 - 312] Pages: 9

DOI: 10.2174/1871527321666220318113635

Price: $65

Abstract

Background: Waterpipe smoking (WP) exposure involves a negative health impact, including memory deficit, which is attributed to the elevation of oxidative stress. Vitamin E (VitE) in combination with swimming exercise exerts protective effects that prevent memory impairment. In the current study, the modulation of WP-induced memory impairment by the combined effect of VitE and swimming exercise (SE) was investigated.

Methods: Animals were exposed to WP one hour/day, five days per week for four weeks. Simultaneously, VitE (100 mg/kg, six days/week for four weeks) was administered via oral gavage, and the rats were made to swim one hour/day, five days/week for four weeks. Changes in memory were evaluated using radial arm water maze (RAWM), and oxidative stress biomarkers were examined in the hippocampus.

Results: WP exposure induced short-term/long-term memory impairment (p<0.05). This impairment was prevented by a combination of VitE with SE (p<0.05). Additionally, this combination normalized the hippocampal catalase, GPx, and GSH/GSSG ratios that were modulated by WP (p<0.05). The combination further reduced TBARs levels below those of the control group (p<0.05).

Conclusion: WP-induced memory impairments were prevented by the combination of VitE with SE. This could be attributed to preserving the hippocampal oxidative mechanism by combining VitE and SE during WP exposure.

Keywords: Waterpipe, hippocampus, memory, swimming exercise, vitamin E, radial arm water maze.

« Previous Next »
Graphical Abstract

[1]
Breland A, Soule E, Lopez A, Ramôa C, El-Hellani A, Eissenberg T. Electronic cigarettes: What are they and what do they do? Ann N Y Acad Sci 2017; 1394(1): 5-30.
[http://dx.doi.org/10.1111/nyas.12977] [PMID: 26774031]
[2]
Maziak W, Nakkash R, Bahelah R, Husseini A, Fanous N, Eissenberg T. Tobacco in the Arab world: Old and new epidemics amidst policy paralysis. Health Policy Plan 2014; 29(6): 784-94.
[http://dx.doi.org/10.1093/heapol/czt055] [PMID: 23958628]
[3]
Alomari MA, Al-sheyab NA. Dual tobacco smoking is the new trend among adolescents: Update from the Irbid-TRY. J Subst Use 2018; 23(1): 92-8.
[http://dx.doi.org/10.1080/14659891.2017.1348559]
[4]
Jawad M, Charide R, Waziry R, Darzi A, Ballout RA, Akl EA. The prevalence and trends of waterpipe tobacco smoking: A systematic review. PLoS One 2018; 13(2): e0192191.
[http://dx.doi.org/10.1371/journal.pone.0192191] [PMID: 29425207]
[5]
Salloum RG, Thrasher JF, Kates FR, Maziak W. Water pipe tobacco smoking in the United States: Findings from the National Adult Tobacco Survey. Prev Med 2015; 71: 88-93.
[http://dx.doi.org/10.1016/j.ypmed.2014.12.012] [PMID: 25535678]
[6]
Minaker LM, Shuh A, Burkhalter RJ, Manske SR. Hookah use prevalence, predictors, and perceptions among Canadian youth: Findings from the 2012/2013 Youth Smoking Survey. Cancer Causes Control 2015; 26(6): 831-8.
[http://dx.doi.org/10.1007/s10552-015-0556-x] [PMID: 25783457]
[7]
World Health Organization. Advisory note: Waterpipe tobacco smoking: Health effects, research needs andrecommended actions for regulators. 2015. Available from: https://www.who.int/publications/i/item/advisory-note-waterpipe-tobacco-smoking-health-effects-research-needs-and-recommended-actions-by-regulators-2nd-ed
[8]
Jukema JB, Bagnasco DE, Jukema RA. Waterpipe smoking: Not necessarily less hazardous than cigarette smoking: Possible consequences for (cardiovascular) disease. Neth Heart J 2014; 22(3): 91-9.
[http://dx.doi.org/10.1007/s12471-013-0501-0] [PMID: 24307377]
[9]
Khabour OF, Alzoubi KH, Eissenberg T, et al. Waterpipe tobacco and cigarette smoking among university students in Jordan. Int J Tuberc Lung Dis 2012; 16(7): 986-92.
[http://dx.doi.org/10.5588/ijtld.11.0764] [PMID: 22525279]
[10]
Badran M, Laher I. Waterpipe (shisha, hookah) smoking, oxidative stress and hidden disease potential. Redox Biol 2020; 34: 101455.
[http://dx.doi.org/10.1016/j.redox.2020.101455] [PMID: 32086009]
[11]
Eissenberg T, Shihadeh A. Waterpipe tobacco and cigarette smoking: Direct comparison of toxicant exposure. Am J Prev Med 2009; 37(6): 518-23.
[http://dx.doi.org/10.1016/j.amepre.2009.07.014] [PMID: 19944918]
[12]
Sibai AM, Tohme RA, Almedawar MM, et al. Lifetime cumulative exposure to waterpipe smoking is associated with coronary artery disease. Atherosclerosis 2014; 234(2): 454-60.
[http://dx.doi.org/10.1016/j.atherosclerosis.2014.03.036] [PMID: 24814409]
[13]
Waziry R, Jawad M, Ballout RA, Al Akel M, Akl EA. The effects of waterpipe tobacco smoking on health outcomes: An updated systematic review and meta-analysis. Int J Epidemiol 2017; 46(1): 32-43.
[PMID: 27075769]
[14]
Alzoubi KH, Khabour OF, Alharahshah EA, Alhashimi FH, Shihadeh A, Eissenberg T. The effect of waterpipe tobacco smoke exposure on learning and memory functions in the rat model. J Mol Neurosci 2015; 57(2): 249-56.
[http://dx.doi.org/10.1007/s12031-015-0613-7] [PMID: 26160697]
[15]
Khabour OF, Alzoubi KH, Al-Sawalha N, Ahmad MB, Shihadeh A, Eissenberg T. The effect of chronic exposure to waterpipe tobacco smoke on airway inflammation in mice. Life Sci 2018; 200: 110-4.
[http://dx.doi.org/10.1016/j.lfs.2018.03.034] [PMID: 29555589]
[16]
Khabour OF, Alzoubi KH, Bani-Ahmad M, Dodin A, Eissenberg T, Shihadeh A. Acute exposure to waterpipe tobacco smoke induces changes in the oxidative and inflammatory markers in mouse lung. Inhal Toxicol 2012; 24(10): 667-75.
[http://dx.doi.org/10.3109/08958378.2012.710918] [PMID: 22906173]
[17]
Ramis MR, Sarubbo F, Terrasa JL, et al. Chronic α-tocopherol increases central monoamines synthesis and improves cognitive and motor abilities in old rats. Rejuvenation Res 2016; 19(2): 159-71.
[http://dx.doi.org/10.1089/rej.2015.1685] [PMID: 26414867]
[18]
Aiguo W, Zhe Y, Gomez-Pinilla F. Vitamin E protects against oxidative damage and learning disability after mild traumatic brain injury in rats. Neurorehabil Neural Repair 2010; 24(3): 290-8.
[http://dx.doi.org/10.1177/1545968309348318] [PMID: 19841436]
[19]
Tagami M, Yamagata K, Ikeda K, et al. Vitamin E prevents apoptosis in cortical neurons during hypoxia and oxygen reperfusion. Lab Invest 1998; 78(11): 1415-29.
[PMID: 9840616]
[20]
Jahanshahi M, Nikmahzar E, Sayyahi A. Vitamin E therapy prevents the accumulation of congophilic amyloid plaques and neurofibrillary tangles in the hippocampus in a rat model of Alzheimer’s disease. Iran J Basic Med Sci 2020; 23(1): 86-92.
[PMID: 32395206]
[21]
Alzoubi KH, Khabour OF, Rashid BA, Damaj IM, Salah HA. The neuroprotective effect of vitamin E on chronic sleep deprivation-induced memory impairment: The role of oxidative stress. Behav Brain Res 2012; 226(1): 205-10.
[http://dx.doi.org/10.1016/j.bbr.2011.09.017] [PMID: 21944940]
[22]
Alzoubi KH, Khabour OF, Salah HA, Hasan Z. Vitamin E prevents high-fat high-carbohydrates diet-induced memory impairment: the role of oxidative stress. Physiol Behav 2013; 119: 72-8.
[http://dx.doi.org/10.1016/j.physbeh.2013.06.011] [PMID: 23769690]
[23]
Khodamoradi N, Komaki A, Salehi I, Shahidi S, Sarihi A. Effect of vitamin E on lead exposure-induced learning and memory impairment in rats. Physiol Behav 2015; 144: 90-4.
[http://dx.doi.org/10.1016/j.physbeh.2015.03.015] [PMID: 25777497]
[24]
Sezer Z, Ekiz Yilmaz T, Gungor ZB, Kalay F, Guzel E. Effects of vitamin E on nicotine-induced lipid peroxidation in rat granulosa cells: Folliculogenesis. Reprod Biol 2020; 20(1): 63-74.
[http://dx.doi.org/10.1016/j.repbio.2019.12.004] [PMID: 31918980]
[25]
Duran M, Ustunyurt E, Kosus A, et al. Does vitamin E prevent tubal damage caused by smoking? A light microscopy and animal study. Eur J Obstet Gynecol Reprod Biol 2014; 175: 149-51.
[http://dx.doi.org/10.1016/j.ejogrb.2014.01.020] [PMID: 24530190]
[26]
He M-A, Cheng L-X, Jiang C-Z, et al. Associations of polymorphism of P22phox C242T, plasma levels of vitamin E, and smoking with coronary heart disease in China. American Heart Journal 2007; 153(4): 640.
[http://dx.doi.org/10.1016/j.ahj.2007.01.002]
[27]
Yang J, Wang L, Chen Z, et al. Antioxidant intervention of smoking-induced lung tumor in mice by vitamin E and quercetin. BMC Cancer 2008; 8(1): 383.
[http://dx.doi.org/10.1186/1471-2407-8-383] [PMID: 19099597]
[28]
Alzoubi KH, Halboup AM, Alomari MA, Khabour OF. The neuroprotective effect of vitamin E on waterpipe tobacco smoking-induced memory impairment: The antioxidative role. Life Sci 2019; 222: 46-52.
[http://dx.doi.org/10.1016/j.lfs.2019.02.050] [PMID: 30817915]
[29]
de Souza CP, Gambeta E, Stern CAJ, Zanoveli JM. Posttraumatic stress disorder-type behaviors in streptozotocin-induced diabetic rats can be prevented by prolonged treatment with vitamin E. Behav Brain Res 2019; 359: 749-54.
[http://dx.doi.org/10.1016/j.bbr.2018.09.008] [PMID: 30219262]
[30]
Yatin SM, Varadarajan S, Butterfield DA. Vitamin E prevents Alzheimer’s amyloid ß-Peptide (1-42)-induced neuronal protein oxidation and reactive oxygen species production. J Alzheimers Dis 2000; 2(2): 123-31.
[http://dx.doi.org/10.3233/JAD-2000-2212] [PMID: 12214102]
[31]
Nakhaee MR, Joukar S, Zolfaghari MR, et al. Effects of endurance exercise training on cardiac dysfunction induced by waterpipe tobacco smoking. Addict Health 2019; 11(2): 100-9.
[PMID: 31321007]
[32]
Zagaar M, Dao A, Levine A, Alhaider I, Alkadhi K. Regular exercise prevents sleep deprivation associated impairment of long-term memory and synaptic plasticity in the CA1 area of the hippocampus. Sleep 2013; 36(5): 751-61.
[http://dx.doi.org/10.5665/sleep.2642] [PMID: 23633758]
[33]
Alomari MA, Khabour OF, Alzoubi KH, Alzubi MA. Forced and voluntary exercises equally improve spatial learning and memory and hippocampal BDNF levels. Behav Brain Res 2013; 247: 34-9.
[http://dx.doi.org/10.1016/j.bbr.2013.03.007] [PMID: 23499703]
[34]
Zhong T, Ren F, Huang CS, et al. Swimming exercise ameliorates neurocognitive impairment induced by neonatal exposure to isoflurane and enhances hippocampal histone acetylation in mice. Neuroscience 2016; 316: 378-88.
[http://dx.doi.org/10.1016/j.neuroscience.2015.12.049] [PMID: 26748054]
[35]
Alzoubi KH, Halboup AM, Alomari MA, Khabour OF. Swimming exercise protective effect on waterpipe tobacco smoking-induced impairment of memory and oxidative stress. Life Sci 2019; 239: 117076.
[http://dx.doi.org/10.1016/j.lfs.2019.117076] [PMID: 31751578]
[36]
Vanzella C, Sanches EF, Odorcyk FK, et al. Forced treadmill exercise prevents spatial memory deficits in aged rats probably through the activation of Na+, K+-ATPase in the hippocampus. Neurochem Res 2017; 42(5): 1422-9.
[http://dx.doi.org/10.1007/s11064-017-2196-x] [PMID: 28210957]
[37]
Loprinzi PD, Ponce P, Zou L, Li H. The counteracting effects of exercise on high-fat diet-induced memory impairment: A systematic review. Brain Sci 2019; 9(6): E145.
[http://dx.doi.org/10.3390/brainsci9060145] [PMID: 31226771]
[38]
Marcelino TB, Longoni A, Kudo KY, et al. Evidences that maternal swimming exercise improves antioxidant defenses and induces mitochondrial biogenesis in the brain of young Wistar rats. Neuroscience 2013; 246: 28-39.
[http://dx.doi.org/10.1016/j.neuroscience.2013.04.043] [PMID: 23639877]
[39]
Liao CF, Yang TY, Chen YH, Yao CH, Way TD, Chen YS. Effects of swimming exercise on nerve regeneration in a rat sciatic nerve transection model. Biomedicine (Taipei) 2017; 7(1): 3.
[http://dx.doi.org/10.1051/bmdcn/2017070103] [PMID: 28474579]
[40]
Khabour OF, Alzoubi KH, Alomari MA, Alzubi MA. Changes in spatial memory and BDNF expression to simultaneous dietary restriction and forced exercise. Brain Res Bull 2013; 90: 19-24.
[http://dx.doi.org/10.1016/j.brainresbull.2012.08.005] [PMID: 23000024]
[41]
Curlik DM II, Shors TJ. Training your brain: Do mental and physical (MAP) training enhance cognition through the process of neurogenesis in the hippocampus? Neuropharmacology 2013; 64: 506-14.
[http://dx.doi.org/10.1016/j.neuropharm.2012.07.027] [PMID: 22898496]
[42]
Llorens-Martín M, Torres-Alemán I, Trejo JL. Exercise modulates insulin-like growth factor 1-dependent and -independent effects on adult hippocampal neurogenesis and behaviour. Mol Cell Neurosci 2010; 44(2): 109-17.
[http://dx.doi.org/10.1016/j.mcn.2010.02.006] [PMID: 20206269]
[43]
Alomari MA, Khabour OF, Alzoubi KH, Alzubi MA. Combining restricted diet with forced or voluntary exercises improves hippocampal BDNF and cognitive function in rats. Int J Neurosci 2016; 126(4): 366-73.
[http://dx.doi.org/10.3109/00207454.2015.1012587] [PMID: 26000806]
[44]
Hasanein P, Shahidi S. Effects of combined treatment with vitamins C and E on passive avoidance learning and memory in diabetic rats. Neurobiol Learn Mem 2010; 93(4): 472-8.
[http://dx.doi.org/10.1016/j.nlm.2010.01.004] [PMID: 20085822]
[45]
Khabour OF, Alzoubi KH, Alomari MA, Alzubi MA. Changes in spatial memory and BDNF expression to concurrent dietary restriction and voluntary exercise. Hippocampus 2010; 20(5): 637-45.
[PMID: 19530223]
[46]
Alzoubi KH, Khabour OF, Salah HA, Abu Rashid BE. The combined effect of sleep deprivation and Western diet on spatial learning and memory: Role of BDNF and oxidative stress. J Mol Neurosci 2013; 50(1): 124-33.
[47]
Alzoubi KH, Mayyas FA, Khabour OF, Bani Salama FM, Alhashimi FH, Mhaidat NM. Chronic melatonin treatment prevents memory impairment induced by chronic sleep deprivation. Mol Neurobiol 2016; 53(5): 3439-47.
[http://dx.doi.org/10.1007/s12035-015-9286-z] [PMID: 26084441]
[48]
Diamond DM, Park CR, Heman KL, Rose GM. Exposing rats to a predator impairs spatial working memory in the radial arm water maze. Hippocampus 1999; 9(5): 542-52.
[http://dx.doi.org/10.1002/(SICI)1098-1063(1999)9:5<542:AID-HIPO8>3.0.CO;2-N] [PMID: 10560925]
[49]
Alquraan L, Alzoubi KH, Hammad H, Rababa’h SY, Mayyas F. Omega-3 fatty acids prevent post-traumatic stress disorder-induced memory impairment. Biomolecules 2019; 9(3): 100.
[http://dx.doi.org/10.3390/biom9030100] [PMID: 30871113]
[50]
Alzoubi KH, Rababa’h AM, Al Yacoub ON. Tempol prevents post-traumatic stress disorder induced memory impairment. Physiol Behav 2018; 184: 189-95.
[http://dx.doi.org/10.1016/j.physbeh.2017.12.002] [PMID: 29217357]
[51]
Al-Sawalha N, Alzoubi K, Khabour O, Alyacoub W, Almahmmod Y, Eissenberg T. Effect of prenatal exposure to waterpipe tobacco smoke on learning and memory of adult offspring rats. Nicotine Tob Res 2018; 20(4): 508-14.
[http://dx.doi.org/10.1093/ntr/ntx142] [PMID: 28637174]
[52]
Al-Sawalha NA, Alzoubi KH, Khabour OF, Alyacoub W, Almahmood Y. Effect of waterpipe tobacco smoke exposure during lactation on learning and memory of offspring rats: Role of oxidative stress. Life Sci 2019; 227: 58-63.
[http://dx.doi.org/10.1016/j.lfs.2019.04.049] [PMID: 31009626]
[53]
Yang J, Jiang LN, Yuan ZL, et al. Impacts of passive smoking on learning and memory ability of mouse offsprings and intervention by antioxidants. Biomed Environ Sci 2008; 21(2): 144-9.
[http://dx.doi.org/10.1016/S0895-3988(08)60020-3] [PMID: 18548854]
[54]
Amos-Kroohs RM, Williams MT, Braun AA, et al. Neurobehavioral phenotype of C57BL/6J mice prenatally and neonatally exposed to cigarette smoke. Neurotoxicol Teratol 2013; 35: 34-45.
[http://dx.doi.org/10.1016/j.ntt.2013.01.001] [PMID: 23314114]
[55]
Wang F, Fangfang Z, Guo X, et al. Effects of volatile organic compounds and carbon monoxide mixtures on learning and memory, oxidative stress, and monoamine neurotransmitters in the brains of mice. Toxicol Ind Health 2018; 34(3): 178-87.
[http://dx.doi.org/10.1177/0748233717747504] [PMID: 29506457]
[56]
Gupta YK, Gupta M, Kohli K. Neuroprotective role of melatonin in oxidative stress vulnerable brain. Indian J Physiol Pharmacol 2003; 47(4): 373-86.
[PMID: 15266948]
[57]
Ahmed M, Alzoubi KH, Khabour OF. Vitamin E prevents the cognitive impairments in post-traumatic stress disorder rat model: Behavioral and molecular study. Psychopharmacology (Berl) 2020; 237(2): 599-607.
[http://dx.doi.org/10.1007/s00213-019-05395-w] [PMID: 31734707]
[58]
El-Elimat T, Alzoubi KH, AbuAlSamen MM, Al Subeh ZY, Graf TN, Oberlies NH. Silymarin prevents memory impairments, anxiety, and depressive-like symptoms in a rat model of post-traumatic stress disorder. Planta Med 2019; 85(1): 32-40.
[http://dx.doi.org/10.1055/a-0710-5673] [PMID: 30153692]
[59]
Nasehi M, Mosavi-Nezhad SM, Khakpai F, Zarrindast MR. The role of omega-3 on modulation of cognitive deficiency induced by REM sleep deprivation in rats. Behav Brain Res 2018; 351: 152-60.
[http://dx.doi.org/10.1016/j.bbr.2018.06.002] [PMID: 29870765]
[60]
Baghcheghi Y, Beheshti F, Shafei MN, et al. The effects of vitamin E on brain derived neurotrophic factor, tissues oxidative damage and learning and memory of juvenile hypothyroid rats. Metab Brain Dis 2018; 33(3): 7193-24.
[PMID: 29290043]
[61]
Csiszar A, Labinskyy N, Podlutsky A, et al. Vasoprotective effects of resveratrol and SIRT1: Attenuation of cigarette smoke-induced oxidative stress and proinflammatory phenotypic alterations. Am J Physiol Heart Circ Physiol 2008; 294(6): H2721-35.
[http://dx.doi.org/10.1152/ajpheart.00235.2008] [PMID: 18424637]
[62]
Di Vincenzo S, Gjomarkaj M, Noordhoek J, et al. Cigarette smoke impairs Sirt1 activity and promotes pro-inflammatory responses in bronchial epithelial cells. Eur Respiratory Soc 2015.
[http://dx.doi.org/10.1183/13993003.congress-2015.PA5105]
[63]
Ma N, Deng TT, Wang Q, et al. Erythromycin regulates cigarette smoke-induced proinflammatory mediator release through sirtuin 1-nuclear factor κB axis in macrophages and mice lungs. Pathobiology 2019; 86(5-6): 237-47.
[64]
Hwang JW, Chung S, Sundar IK, et al. Cigarette smoke-induced autophagy is regulated by SIRT1-PARP-1-dependent mechanism: Implication in pathogenesis of COPD. Arch Biochem Biophys 2010; 500(2): 203-9.
[http://dx.doi.org/10.1016/j.abb.2010.05.013] [PMID: 20493163]
[65]
Michán S, Li Y, Chou MM, et al. SIRT1 is essential for normal cognitive function and synaptic plasticity. J Neurosci 2010; 30(29): 9695-707.
[http://dx.doi.org/10.1523/JNEUROSCI.0027-10.2010] [PMID: 20660252]
[66]
Saboori S, Koohdani F, Nematipour E, et al. Beneficial effects of omega-3 and vitamin E coadministration on gene expression of SIRT1 and PGC1α and serum antioxidant enzymes in patients with coronary artery disease. Nutr Metab Cardiovasc Dis 2016; 26(6): 489-94.
[http://dx.doi.org/10.1016/j.numecd.2015.11.013] [PMID: 27033026]
[67]
Vargas-Ortiz K, Pérez-Vázquez V, Macías-Cervantes MH. Exercise and sirtuins: A way to mitochondrial health in skeletal muscle. Int J Mol Sci 2019; 20(11): E2717.
[http://dx.doi.org/10.3390/ijms20112717] [PMID: 31163574]
[68]
Zillikens MC, van Meurs JB, Rivadeneira F, et al. Interactions between dietary vitamin E intake and SIRT1 genetic variation influence body mass index. Am J Clin Nutr 2010; 91(5): 1387-93.
[http://dx.doi.org/10.3945/ajcn.2009.28627] [PMID: 20335544]
[69]
Asha Devi S, Manjula KR, Subramanyam MV. Protective role of vitamins E and C against oxidative stress caused by intermittent cold exposure in aging rat’s frontoparietal cortex. Neurosci Lett 2012; 529(2): 155-60.
[http://dx.doi.org/10.1016/j.neulet.2012.09.041] [PMID: 23026027]
[70]
Gurel A, Coskun O, Armutcu F, Kanter M, Ozen OA. Vitamin E against oxidative damage caused by formaldehyde in frontal cortex and hippocampus: biochemical and histological studies. J Chem Neuroanat 2005; 29(3): 173-8.
[http://dx.doi.org/10.1016/j.jchemneu.2005.01.001] [PMID: 15820619]
[71]
Al-Eitan LN, Alzoubi KH, Al-Smadi LI, Khabour OF. Vitamin E protects against cisplatin-induced genotoxicity in human lymphocytes. Toxicol In Vitro 2020; 62: 104672.
[http://dx.doi.org/10.1016/j.tiv.2019.104672] [PMID: 31629897]
[72]
Naderi R, Mohaddes G, Mohammadi M, Ghaznavi R, Ghyasi R, Vatankhah AM. Voluntary exercise protects heart from oxidative stress in diabetic rats. Adv Pharm Bull 2015; 5(2): 231-6.
[http://dx.doi.org/10.15171/apb.2015.032] [PMID: 26236662]
[73]
Delwing-de Lima D, Ulbricht ASSF, Werlang-Coelho C, et al. Effects of two aerobic exercise training protocols on parameters of oxidative stress in the blood and liver of obese rats. J Physiol Sci 2018; 68(5): 699-706.
[http://dx.doi.org/10.1007/s12576-017-0584-2] [PMID: 29222739]
[74]
Ávila LC, Bruggemann TR, Bobinski F, et al. Effects of high-intensity swimming on lung inflammation and oxidative stress in a murine model of DEP-induced injury. PLoS One 2015; 10(9): e0137273.
[http://dx.doi.org/10.1371/journal.pone.0137273] [PMID: 26332044]
[75]
Alqudah MAY, Alzoubi KH, Ma’abrih GM, Khabour OF. Vitamin C prevents memory impairment induced by waterpipe smoke: Role of oxidative stress. Inhal Toxicol 2018; 30(4-5): 141-8.
[http://dx.doi.org/10.1080/08958378.2018.1474977] [PMID: 29788804]
[76]
Al-Sawalha NA, Al-Filali MS, Alzoubi KH, Khabour OF. Effect of prenatal waterpipe tobacco smoke exposure on cardiac biomarkers in adult offspring rats. J Cardiovasc Pharmacol Ther 2019; 24(6): 567-74.
[http://dx.doi.org/10.1177/1074248419849424] [PMID: 31106579]
[77]
Cordeira J, Kolluru SS, Rosenblatt H, Kry J, Strecker RE, McCarley RW. Learning and memory are impaired in the object recognition task during metestrus/diestrus and after sleep deprivation. Behav Brain Res 2018; 339: 124-9.
[http://dx.doi.org/10.1016/j.bbr.2017.11.033] [PMID: 29180134]
[78]
Scharfman HE, Mercurio TC, Goodman JH, Wilson MA, MacLusky NJ. Hippocampal excitability increases during the estrous cycle in the rat: A potential role for brain-derived neurotrophic factor. J Neurosci 2003; 23(37): 11641-52.
[http://dx.doi.org/10.1523/JNEUROSCI.23-37-11641.2003] [PMID: 14684866]
[79]
Alkadhi KA, Alzoubi KH. Comparison of effects of spatial and non-spatial memory acquisition on the CaMKII pathway during hypothyroidism and nicotine treatment. Mol Neurobiol 2020; 57(4): 1930-7.
[http://dx.doi.org/10.1007/s12035-019-01865-6] [PMID: 31900862]

Rights & Permissions Print Cite
Article Metrics
16
2
© 2024 Bentham Science Publishers | Privacy Policy