Wild pistachio (Pistacia atlantica mutica) oil improve metabolic syndrome features in rats with high fructose ingestion

Document Type: Original Article

Authors

1 Department of Clinical Nutrition, School of Nutrition and food sciences, Shiraz University of Medical Sciences, Shiraz, Iran

2 Nutrition Research Center, Department of Clinical Nutrition, School of Nutrition and Food Sciences, Shiraz University of Medical Sciences, Shiraz, Iran

3 Department of Food Science and Technology, School of Agriculture, Shiraz University, Shiraz, Iran

4 Stem Cell and Transgenic Research Center, Shiraz University of Medical Sciences, Shiraz, Iran

Abstract

Objective(s): Metabolic syndrome is a multiplex risk factor for diabetes and cardiovascular disease. Since some dietary fats such as mono-unsaturated fatty acids (MUFA) modify metabolic syndrome components the aim of the present study was to evaluate  the preventive effects of mixture, kernel and hull oils of wild pistachio (WP) (Pistacia atlantica mutica) as good sources of MUFA on different features of this abnormality in rats under induction.
Materials and Methods: In this study rats were randomly assigned to six groups with 12 animals per group. Metabolic syndrome was induced by fructose solution in groups 2, 3, 4, 5, and 6. Group 3 received sunflower oil and groups 4, 5, and 6 received mixture, hull and kernel oils of WP (2 ml/kg/day), respectively, for 10 weeks. Then, lipid profiles, glycemic indices, oxidative stress and inflammatory parameters were measured using standard laboratory tests.
Results: Different forms of WP oil induced hypotriglyceridemia, but the hypocholesterolemia effect was seen only in the mixed and kernel oil groups. Kernel oil also significantly reduced LDL and HDL cholesterol (P<0.05). In addition, mixed and kernel oils notably decreased glycemic indices (fasting blood glucose and insulin resistance) compared with the fructose group. Serum insulin levels were significantly increased in the kernel oil group (P<0.05). All WP oils also significantly decreased inflammation (IL-6).
Conclusion: The results showed that the consumption of WP kernel oil may have beneficial effects on preventing hyperglycemia, hypertriglyceridemia, hypercholesterolemia, inflammation and pancreatic secretory disorders.

Keywords

Main Subjects


1. Grundy SM, Brewer HB, Cleeman JI, Smith SC, Lenfant C. Definition of metabolic syndrome. Arterioscler Thromb Vasc Biol 2004;109:433-438.
2. Gillingham LG, Harris-Janz S, Jones PJ. Dietary monounsaturated fatty acids are protective against metabolic syndrome and cardiovascular disease risk factors. Lipids 2011;46:209-228.
3. Alberti KGM, Zimmet P, Shaw J. The metabolic syndrome—a new worldwide definition. Lancet 2005;366:1059-1062.
4. Carroll S, Dudfield M. What is the relationship between exercise and metabolic abnormalities? Sports Med 2004;34:371-418.
5. Cheal KL, Abbasi F, Lamendola C, McLaughlin T, Reaven GM, Ford ES. Relationship to insulin resistance of the adult treatment panel III diagnostic criteria for identification of the metabolic syndrome. Diabetes 2004;53:1195-1200.
6. Fujita K, Nishizawa H, Funahashi T, Shimomura I, Shimabukuro M. Systemic oxidative stress is associated with visceral fat accumulation and the metabolic syndrome. Circ J 2006;70:1437-1442.
7. Riccardi G, Rivellese A. Dietary treatment of the metabolic syndrome—the optimal diet. Br J Nutr 2000;83:143-148.
8. Ford ES, Mokdad AH, Giles WH, Brown DW. The metabolic syndrome and antioxidant concentrations. Diabetes 2003;52:2346-2352.
9. Kastorini C-M, Milionis HJ, Esposito K, Giugliano D, Goudevenos JA, Panagiotakos DB. The effect of mediterranean diet on metabolic syndrome and its components: a meta-analysis of 50 studies and 534,906 individuals. J Am Coll Cardiol 2011;57:1299-1313.
10. Nejabat M, Negahdarsaber M, Ghahari G. Range of soil and climate characteristics appropriate for Pistacia atlantica forest development an d rehabilitation (case study: Fars province, Iran). JWLD 2017;32:71-78.
11. Pourreza M, Shaw JD, Zangeneh H. Sustainability of wild pistachio (Pistacia atlantica Desf.) in Zagros forests, Iran. Forest Ecology and Management 2008;255:3667-3671.
12. Farhoosh R, Khodaparast MHH, Sharif A. Bene hull oil as a highly stable and antioxidative vegetable oil. Eur J Lipid Sci 2009;111:1259-1265.
13. Memariani Z, Sharifzadeh M, Bozorgi M, Hajimahmoodi M, Farzaei MH, Gholami M, et al. Protective effect of essential oil of Pistacia atlantica Desf. On peptic ulcer: role of α-pinene. J Tradit Chin Med 2017;37:57-63.
14. Hashemnia M, Nikousefat Z, Yazdani-Rostam M. Antidiabetic effect of Pistacia atlantica and Amygdalus scoparia in streptozotocin-induced diabetic mice. Comp Clin Pathol 2015;24:1301-1306.
15. Tanideh N, Masoumi S, Hosseinzadeh M, Safarpour AR, Erjaee H, Koohi-Hosseinabadi O, et al. Healing effect of Pistacia atlantica fruit oil extract in acetic Acid-induced colitis in rats. Iran J Med Sci 2014;39:522-528.
16. Arami S, Mojaddadi M, Pourabbas R, Chitsaz M, Delazar A, Mobayen H. The effect of Pistacia atlantica Var. mutica mouthwash on dental plaque bacteria and subgingival microorganisms: a randomized and controlled triple-blind study. Drug Res 2015;65:463-467.
17. Saber-Tehrani M, Givianrad M, Aberoomand-Azar P, Waqif-Husain S, Jafari Mohammadi S. Chemical composition of Iran’s Pistacia atlantica cold-pressed oil. J Chem 2012;2013:1-6.
18. Barbosa C, Albuquerque E, Faria E, Oliveira H, Castilho L. Opposite lipemic response of Wistar rats and C57BL/6 mice to dietary glucose or fructose supplementation. Braz J Med Biol Res 2007;40:323-331.
19. Zal F, Mostafavi‐Pour Z, Vessal M. Comparison of the effects of vitamin e and/or quercetin in attenuating chronic cyclosporine a‐induced nephrotoxicity in male rats. Clin Exp Pharmacol Physiol 2007;34:720-724.
20. Matthews D, Hosker J, Rudenski A, Naylor B, Treacher D, Turner R. Homeostasis model assessment: insulin resistance and β-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985;28:412-419.
21. Rozner S, Garti N. The activity and absorption relationship of cholesterol and phytosterols. Colloids Surf A 2006;282:435-456.
22. Włodarek D. The mechanisms of blood LDL-cholesterol lowering by phytosterols-a review. Rocz Panstw Zakl Hig 2007;58:47-51.
23. Berger A, Jones PJ, Abumweis SS. Plant sterols: factors affecting their efficacy and safety as functional food ingredients. Lipids Health Dis 2004;3:5-23.
24. Law M. Plant sterol and stanol margarines and health. BMJ 2000;320:861-864.
25. Farquhar JW, Smith RE, Dempsey ME. The effect of beta sitosterol on the serum lipids of young men with arteriosclerotic heart disease. Circulation 1956;14:77-82.
26. Alberti KGMM, Zimmet P, Shaw J. Metabolic syndrome—a new world‐wide definition. A consensus statement from the international diabetes federation. Diabet Med 2006;23:469-480.
27. Ginsberg HN. New perspectives on atherogenesis. Circulation 2002;106:2137-2142.
28. Assy N, Nassar F, Nasser G, Grosovski M. Olive oil consumption and non-alcoholic fatty liver disease. World J Gastroenterol 2009;15:1809-1815.
29. Maeda H, Hosokawa M, Sashima T, Miyashita K. Dietary combination of fucoxanthin and fish oil attenuates the weight gain of white adipose tissue and decreases blood glucose in obese/diabetic KK-Ay mice. J Agric Food Chem 2007;55:7701-7706.
30. Mcnamara DJ. Dietary fatty acids, lipoproteins, and cardiovascular disease. Adv Food Nutr Res 1992;36:253-351.
31. Kris-Etherton PM, Pearson TA, Wan Y, Hargrove RL, Moriarty K, Fishell V, et al. High–monounsaturated fatty acid diets lower both plasma cholesterol and triacylglycerol concentrations. Am J Clin Nutr 1999;70:1009-1015.
32. Clarke SD. Polyunsaturated fatty acid regulation of gene transcription: a molecular mechanism to improve the metabolic syndrome. J Nutr 2001;131:1129-1132.
33. Karadag MK, Akbulut M. Low HDL levels as the most common metabolic syndrome risk factor in heart failure. Int Heart J 2009;50:571-580.
34. Freitas H, Barbosa E, Rosa F, Lima A, Mansur A. Association of HDL cholesterol and triglycerides with mortality in patients with heart failure. Braz J Med Biol Res 2009;42:420-425.
35. Mattson FH, Grundy SM. Comparison of effects of dietary saturated, monounsaturated, and polyunsaturated fatty acids on plasma lipids and lipoproteins in man. J Lipid Res 1985;26:194-202.
36. Saeb M, Nazifi S, Mirzaei A. Studies on the effects of turpentine oil on the serum concentration of lipids and lipoproteins of female rabbits. SSU J 2004;12:42-50.
37. Lira FS, Rosa JC, Cunha CA, Ribeiro EB, do Nascimento CO, Oyama LM, et al. Supplementing alpha-tocopherol (vitamin E) and vitamin D3 in high fat diet decrease IL-6 production in murine epididymal adipose tissue and 3T3-L1 adipocytes following LPS stimulation. Lipids Health Dis 2011;10:37-42.
38. Moreno JJ, Carbonell T, Sanchez T, Miret S, Mitjavila MT. Olive oil decreases both oxidative stress and the production of arachidonic acid metabolites by the prostaglandin G/H synthase pathway in rat macrophages. J  Nutr 2001;131:2145-2149.
39. Fitó M, Cladellas M, De la Torre R, Marti J, Munoz D, Schröder H, et al. Anti-inflammatory effect of virgin olive oil in stable coronary disease patients: a randomized, crossover, controlled trial. Eur J Clin Nutr 2008;62:570-574.
40. Igoillo-Esteve M, Marselli L, Cunha D, Ladrière L, Ortis F, Grieco FA, et al. Palmitate induces a pro-inflammatory response in human pancreatic islets that mimics CCL2 expression by beta cells in type 2 diabetes. Diabetologia 2010;53:1395-1405.
41. Eizirik DL, Colli ML, Ortis F. The role of inflammation in insulitis and β-cell loss in type 1 diabetes. Nat Rev Endocrinol 2009;5:219-226.
42. Toul F, Belyagoubi-Benhammou N, Zitouni A, Atik-Bekkara F. Antioxidant activity and phenolic profile of different organs of Pistacia atlantica Desf. subsp. atlantica from Algeria. Nat Prod Res 2017;31:718-723.
43. Maedler K, Oberholzer J, Bucher P, Spinas GA, Donath MY. Monounsaturated fatty acids prevent the deleterious effects of palmitate and high glucose on human pancreatic β-cell turnover and function. Diabetes 2003;52:726-733.
44. Garg A. High monounsaturated fat diet for diabetic patients: Is it time to change the current dietary recommendations? Diabetes Care 1994;17:242-246.
45. Rocca AS, LaGreca J, Kalitsky J, Brubaker PL. Monounsaturated fatty acid diets improve glycemic tolerance through increased secretion of glucagon-like peptide-1. Endocrinology 2001;142:1148-1155.
46. Sato K, Arai H, Mizuno A, Fukaya M, Sato T, Koganei M, et al. Dietary palatinose and oleic acid ameliorate disorders of glucose and lipid metabolism in Zucker fatty rats. J Nutr 2007;137:1908-1915.
47. Bermudez B, Lopez S, Ortega A, M Varela L, M Pacheco Y, Abia R, et al. Oleic acid in olive oil: from a metabolic framework toward a clinical perspective. Curr Pharm Des 2011;17:831-843.
48. Rolo AP, Palmeira CM. Diabetes and mitochondrial function: role of hyperglycemia and oxidative stress. Toxicol Appl Pharmacol 2006;212:167-178.
49. Kaneto H, Kajimoto Y, Miyagawa J-i, Matsuoka T-a, Fujitani Y, Umayahara Y, et al. Beneficial effects of antioxidants in diabetes: possible protection of pancreatic beta-cells against glucose toxicity. Diabetes 1999;48:2398-2406.
50. Belyagoubi-Benhammou N, Belyagoubi L, El Zerey-Belaskri A, Atik Bekkara F. In vitro antioxidant properties of flavonoid fractions from Pistacia atlantica Desf. subsp. atlantica fruit using five techniques. J Mater Environ Sci 2014;6:1118-1125.
51. Farhoosh R, Tavakoli J, Khodaparast MHH. Chemical composition and oxidative stability of kernel oils from two current subspecies of Pistacia atlantica in Iran. J Am Oil Chem’ Soc 2008;85:723-729.
52. Rashidi S, Askari N, Abbasnejad M. Anxiolytic-like effect of Pistacia atlantica fruit in intact and gonadectomized rats subjected to chronic stress. JOHE 2014;3:152-159.
53. Farahpour MR, Mirzakhani N, Doostmohammadi J, Ebrahimzadeh M. Hydroethanolic Pistacia atlantica hulls extract improved wound healing process; evidence for mast cells infiltration, angiogenesis and RNA stability. Int J Surg 2015;17:88-98.
54. Harborne A. Phytochemical methods a guide to modern techniques of plant analysis: Springer Science & Business Media; 1998.
55. Dai J, Mumper RJ. Plant phenolics: extraction, analysis and their antioxidant and anticancer properties. Molecules 2010;15:7313-7352.