Chronic Pistachio Pretreatment Alters the Morphology of CA1 Hippocampus Neurons Following Transient Focal Cerebral Ischemia in Rats

Main Article Content

Mohammad Reza Afarinesh
Hossein Pourmobini
Ali Shamsara
Seyed Hasan Eftekhar-Vaghefi
Majid Asadi-Shekaari

Keywords

Pistacia vera, Stroke, Antioxidant, Anti-inflammatory, Cerebral ischemia.

Abstract

Abstract


Background: Consumption of antioxidants is effective on reducing the damage caused by cerebral ischemia.


Objectives: We investigated the effect of Pistacia vera (pistachio) pretreatment on the morphology of the cornu ammonis (CA1) region of hippocampus neurons of the rats' hippocampus following transient focal cerebral occlusion of the middle cerebral artery (MCA).


Methods: In this study, 60 male Wistar rats were divided into 3 groups of control, ischemia, and pretreatment with pistachio (fed with pistachio at 6% of the diet for a five-week duration before the right MCA occlusion). Neurological scores of the rats were assessed using Baderson rating. Thereafter, the animals’ balance and muscle power were assessed by Rotarod and forelimb wire-grip strength tests, respectively. Finally, histopathological and morphometrical characteristics of hippocampal neurons were studied using Hematoxylin-Eosin method.


Results: Neurological scores of the ischemia group significantly decreased compared to the control group (p<0.05), while pretreatment with pistachio significantly improved Baderson rating scores compared to the ischemia group (p<0.05). Although stroke significantly decreased the balance and muscular strength in the studied rats compared to the normal rats (p<0.05), pistachio’s exposure significantly increased the balance and muscular strength compared to the ischemia group (p<0.05). Additionally, a significant decrease was observed in the volume of stroke and neuronal degradation in pistachio-treated rats compared with the ischemia group (p<0.05).


Conclusions: Pistachio consumption reduces the volume of infarction and neuronal damage and improves neurological disorders after ischemia. Therefore, pretreatment with pistachio would have a protective effect against stroke.

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References

1. Fisher M, Feuerstein G, Howells D W, Hurn P D, Kent T A, Savitz S I, et al. Update of the stroke therapy academic industry roundtable preclinical recommendations. Stroke. 2009. 40: 2244-2250.
2. Doyle K P, Simon R P, Stenzel-Poore M P. Mechanisms of ischemic brain damage. Neuropharmacology. 2008. 55: 310-318.
3. Yasuhara T, Hara K, Maki M, Masuda T, Sanberg C D, Sanberg P R, et al. Dietary supplementation exerts neuroprotective effects in ischemic stroke model. Rejuvenation research. 2008. 11: 201-214.
4. Kokaia Z, Lindvall O. Neurogenesis after ischaemic brain insults. Curr. Opin. Neurobiol. 2003. 13: 127-132.
5. Kanemitsu H, Nakagomi T, Tamura A, Tsuchiya T, Kono G, Sano K. Differences in the extent of primary ischemic damage between middle cerebral artery coagulation and intraluminal occlusion models. J. Cereb. Blood Flow Metab. 2002. 22: 1196-1204.
6. Liu Y, Belayev L, Zhao W, Busto R, Belayev A, Ginsberg M D. Neuroprotective effect of treatment with human albumin in permanent focal cerebral ischemia: histopathology and cortical perfusion studies. Eur. J. Pharmacol. 2001. 428: 193-201.
7. Alzaga A G, Cerdan M, Varon J, Bigler E D, Ryser D K, Gandhi P, et al. Trauma and rehabilitation. Brain Inj. 2006. 20: 889-894.
8. Zhang X, Shan P, Otterbein L E, Alam J, Flavell R A, Davis R J, et al. Carbon monoxide inhibition of apoptosis during ischemia-reperfusion lung injury is dependent on the p38 mitogen-activated protein kinase pathway and involves caspase 3. Journal of Biological Chemistry. 2003. 278: 1248-1258.
9. Tsokou A, Georgopoulou K, Melliou E, Magiatis P, Tsitsa E. Composition and enantiomeric analysis of the essential oil of the fruits and the leaves of Pistacia vera from Greece. Molecules. 2007. 12: 1233-1239.
10. Pahlavan Y, Sepehri G, Sheibani V, Afarinesh Khaki M, Gojazadeh M, Pahlavan B, et al. Study the antinociceptive effect of intracerebroventricular injection of aqueous extract of origanum vulgare leaves in rat: possible involvement of opioid system. Iran J Basic Med Sci. 2013. 16: 1109-13.
11. Tokuşoglu Ö, Ünal M K, Yemiş F. Determination of the phytoalexin resveratrol (3, 5, 4 ‘-trihydroxystilbene) in peanuts and pistachios by high-performance liquid chromatographic diode array (HPLC-DAD) and gas chromatography− mass spectrometry (GC-MS). J. Agric. Food Chem. 2005. 53: 5003-5009.
12. Rajaei A, Barzegar M, Mobarez A M, Sahari M A, Esfahani Z H. Antioxidant, anti-microbial and antimutagenicity activities of pistachio (Pistachia vera) green hull extract. Food Chem. Toxicol. 2010. 48: 107-112.
13. Tomaino A, Martorana M, Arcoraci T, Monteleone D, Giovinazzo C, Saija A. Antioxidant activity and phenolic profile of pistachio (Pistacia vera L., variety Bronte) seeds and skins. Biochimie. 2010. 92: 1115-1122.
14. Sinha K, Chaudhary G, Gupta Y K. Protective effect of resveratrol against oxidative stress in middle cerebral artery occlusion model of stroke in rats. Life sciences. 2002. 71: 655-665.
15. Mobli H, Oghabi H, Alimardani R. Study of the strength properties of pistachio nuts and cluster stem joints for the design and development of a harvesting machine. Int Agrophys. 2004. 18.
16. Gentile C, Tesoriere L, Butera D, Fazzari M, Monastero M, Allegra M, et al. Antioxidant activity of Sicilian pistachio (Pistacia vera L. var. Bronte) nut extract and its bioactive components. J. Agric. Food Chem. 2007. 55: 643-648.
17. Mansouri S M T, Naghizadeh B, Hosseinzadeh H. The effect of Pistacia vera L. gum extract on oxidative damage during experimental cerebral ischemia-reperfusion in rats. Iran. Biomed. J. 2005. 9: 181-185.
18. Aschoff J, von Goetz C, KI. H. Restricted Feeding in Rats: Effects of Varying Feeding Cycles 1, 2. Z. Tierpsychol. 1983. 63: 91-111.
19. Longa E Z, Weinstein P R, Carlson S, Cummins R. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke. 1989. 20: 84-91.
20. Shamsara A, Sheibani V, Esmaeilpour K, Eslaminejad T, Nematollahi-Mahani S N, Coadministration of the human umbilical cord matrix-derived mesenchymal cells and aspirin alters postischemic brain injury in rats. 2015, Elsevier. p. 2005-2016.
21. Bederson J B, Pitts L H, Tsuji M, Nishimura M C, Davis R L, Bartkowski H. Rat middle cerebral artery occlusion: evaluation of the model and development of a neurologic examination. Stroke. 1986. 17: 472-476.
22. Belayev L, Busto R, Zhao W, Ginsberg M D. Quantitative evaluation of blood-brain barrier permeability following middle cerebral artery occlusion in rats. Brain Res. 1996. 739: 88-96.
23. Rizk N N, Rafols J, Dunbar J C. Cerebral ischemia induced apoptosis and necrosis in normal and diabetic rats. Brain Res. 2005. 1053: 1-9.
24. Bozorgi M, Memariani Z, Mobli M, Salehi Surmaghi M H, Shams-Ardekani M R, Rahimi R. Five Pistacia species (P. vera, P. atlantica, P. terebinthus, P. khinjuk, and P. lentiscus): a review of their traditional uses, phytochemistry, and pharmacology. Sci. World J. 2013. 2013.
25. MacRae H S H, Mefferd K M. Dietary antioxidant supplementation combined with quercetin improves cycling time trial performance. Int. J. Sport Nutr. Exerc. Metab. 2006. 16: 405-419.
26. Schwarz N A, Blahnik Z J, Prahadeeswaran S, McKinley-Barnard S K, Holden S L, Waldhelm A. (-)-Epicatechin Supplementation Inhibits Aerobic Adaptations to Cycling Exercise in Humans. Front. Nutr. 2018. 5: 132.
27. Zamanian M, Hajizadeh M, Shamsizadeh A, Moemenzadeh M, Amirteimouri M, Elshiekh M, et al. Effects of naringin on physical fatigue and serum MMP-9 concentration in female rats. Pharmaceutical biology. 2017. 55: 423-427.
28. Wang Q, Xu J, Rottinghaus G E, Simonyi A, Lubahn D, Sun G Y, et al. Resveratrol protects against global cerebral ischemic injury in gerbils. Brain Res. 2002. 958: 439-447.
29. Ohyama H, Hosomi N, Takahashi T, Mizushige K, Kohno M. Thrombin inhibition attenuates neurodegeneration and cerebral edema formation following transient forebrain ischemia. Brain Res. 2001. 902: 264-271.
30. Ozben T, Balkan E, Balkan S, Serteser M, Gأ¼mأ¼slأ¼ S. Effects of MK-801 on nitrite and cGMP levels during focal cerebral ischemia in rats. Nitric Oxide. 2005. 13: 210-215.
31. Hakimizadeh E, Jandaghi F, Hajmohammadi M, Fatemi I, Kaeidi A, Shamsizadeh A. Pistachio extract improves neurocognitive behaviors in ovariectomized mice. RJP. 2019. 6: 45-51.
32. Ammari M, Othman H, Hajri A, Sakly M, Abdelmelek H. Pistacia lentiscus oil attenuates memory dysfunction and decreases levels of biomarkers of oxidative stress induced by lipopolysaccharide in rats. Brain Res. Bull. 2018. 140: 140-147.
33. Ramassamy C. Emerging role of polyphenolic compounds in the treatment of neurodegenerative diseases: a review of their intracellular targets. Eur. J. Pharmacol. 2006. 545: 51-64.
34. Lipton P. Ischemic cell death in brain neurons. Physiological reviews. 1999. 79: 1431-1568.
35. Elston G N, Elston A, Freire M A M, Leal W G, Dias I A, Pereira Jr A, et al. Specialization of pyramidal cell structure in the visual areas V1, V2 and V3 of the South American rodent, Dasyprocta primnolopha. Brain Res. 2006. 1106: 99-110.
36. Nazifi S, Saeb M, Sepehrimanesh M, Poorgonabadi S. The effects of wild pistachio oil on serum leptin, thyroid hormones, and lipid profile in female rats with experimental hypothyroidism. Comp Clin Path. 2012. 21: 851-857.
37. Wang Y, Chang C-F, Chou J, Chen H-L, Deng X, Harvey B K, et al. Dietary supplementation with blueberries, spinach, or spirulina reduces ischemic brain damage. Experimental neurology. 2005. 193: 75-84.
38. Salah S M, Jäger A K. Screening of traditionally used Lebanese herbs for neurological activities. J Ethnopharmacol. 2005. 97: 145-149.
39. Yousfi M, Nedjmi B, Bellal R, Bertal D B, Palla G. Fatty acids and sterols of Pistacia atlantica fruit oil. Journal of the American Oil Chemists' Society. 2002. 10: 1049-1050.
40. Orhan I, Küpeli E, Aslan M, Kartal M, Yesilada E. Bioassay-guided evaluation of anti-inflammatory and antinociceptive activities of pistachio, Pistacia vera L. J Ethnopharmacol. 2006. 105: 235-240.
41. Kay C D, Gebauer S K, West S G, Kris-Etherton P M. Pistachios increase serum antioxidants and lower serum oxidized-LDL in hypercholesterolemic adults. J. Nutr. 2010. 140: 1093-1098.
42. Ros E. Health benefits of nut consumption. Nutrients. 2010. 2: 652-682.