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Published in: BMC Complementary Medicine and Therapies 1/2017

Open Access 01-12-2017 | Research article

The effect of pomegranate fresh juice versus pomegranate seed powder on metabolic indices, lipid profile, inflammatory biomarkers, and the histopathology of pancreatic islets of Langerhans in streptozotocin-nicotinamide induced type 2 diabetic Sprague–Dawley rats

Authors: Seyedeh Zeinab Taheri Rouhi, Md. Moklesur Rahman Sarker, Asmah Rahmat, Saad Ahmed Alkahtani, Fauziah Othman

Published in: BMC Complementary Medicine and Therapies | Issue 1/2017

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Abstract

Background

Type 2 diabetes mellitus (T2DM) is associated with hyperglycemia, inflammatory disorders and abnormal lipid profiles. Several functional foods have therapeutic potential to treat chronic diseases including diabetes. The therapeutic potential of pomegranate has been stated by multitudinous scientists. The present study aimed to evaluate the effects of pomegranate juice and seed powder on the levels of plasma glucose and insulin, inflammatory biomarkers, lipid profiles, and health of the pancreatic islets of Langerhans in streptozotocin (STZ)-nicotinamide (NAD) induced T2DM Sprague Dawley (SD) rats.

Methods

Forty healthy male SD rats were induced to diabetes with a single dose intra-peritoneal administration of STZ (60 mg/kg b.w.) - NAD (120 mg/kg b.w.). Diabetic rats were orally administered with 1 mL of pomegranate fresh juice (PJ) or 100 mg pomegranate seed powder in 1 mL distilled water (PS), or 5 mg/kg b.w. of glibenclamide every day for 21 days. Rats in all groups were sacrificed on day 22. The obtained data was analyzed by SPSS software (v: 22) using One-way analysis of variance (ANOVA).

Results

The results showed that PJ and PS treatment had slight but non-significant reduction of plasma glucose concentration, and no impact on plasma insulin compared to diabetic control (DC) group. PJ lowered the plasma total cholesterol (TC) and triglyceride (TG) significantly, and low-density lipoproteins (LDL) non-significantly compared to DC group. In contrast, PS treatment significantly raised plasma TC, LDL, and high-density lipoproteins (HDL) levels compared to the DC rats. Moreover, the administration of PJ and PS significantly reduced the levels of plasma inflammatory biomarkers, which were actively raised in diabetic rats. Only PJ treated group showed significant repairment and restoration signs in islets of Langerhans. Besides, PJ possessed preventative impact against 2,2-diphenyl-1-picrylhydrazyl (DPPH) radicals almost 2.5 folds more than PS.

Conclusions

Our findings suggest that active constituents with high antioxidant properties present in PJ are responsible for its anti-hyperlipidemic and anti-inflammatory effects, likewise the restoration effect on the damaged islets of Langerhans in experimental rats. Hence, the pharmacological, biochemical, and histopathological profiles of PJ treated rats obviously indicated its helpful effects in amelioration of diabetes-associated complications.
Literature
1.
go back to reference Association AD. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2016;39(Supplement 1):S13–22.CrossRef Association AD. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2016;39(Supplement 1):S13–22.CrossRef
2.
go back to reference Johansen JS, Harris AK, Rychly DJ, Ergul A. Oxidative stress and the use of antioxidants in diabetes: linking basic science to clinical practice. Cardiovasc Diabetol. 2005;4:5.CrossRefPubMedPubMedCentral Johansen JS, Harris AK, Rychly DJ, Ergul A. Oxidative stress and the use of antioxidants in diabetes: linking basic science to clinical practice. Cardiovasc Diabetol. 2005;4:5.CrossRefPubMedPubMedCentral
3.
go back to reference Sunagawa M, Shimada S, Zhang Z, Oonishi A, Nakamura M, Kosugi T. Plasma insulin concentration was increased by long-term ingestion of guava juice in spontaneous non-insulin-dependent diabetes mellitus (NIDDM) rats. J Health Sci. 2004;50:674–8.CrossRef Sunagawa M, Shimada S, Zhang Z, Oonishi A, Nakamura M, Kosugi T. Plasma insulin concentration was increased by long-term ingestion of guava juice in spontaneous non-insulin-dependent diabetes mellitus (NIDDM) rats. J Health Sci. 2004;50:674–8.CrossRef
4.
go back to reference Opara UL, Al-Ani MR. Antioxidant contents of pre-packed fresh-cut versus whole fruit and vegetables. Br Food J. 2010;112:797–810.CrossRef Opara UL, Al-Ani MR. Antioxidant contents of pre-packed fresh-cut versus whole fruit and vegetables. Br Food J. 2010;112:797–810.CrossRef
5.
go back to reference Scalbert A, Manach C, Morand C, Rémésy C, Jiménez L. Dietary polyphenols and the prevention of diseases. Crit Rev Food Sci Nutr. 2005;45:287–306.CrossRefPubMed Scalbert A, Manach C, Morand C, Rémésy C, Jiménez L. Dietary polyphenols and the prevention of diseases. Crit Rev Food Sci Nutr. 2005;45:287–306.CrossRefPubMed
6.
go back to reference Waltner-Law ME, Wang XL, Law BK, Hall RK, Nawano M, Granner DK. Epigallocatechin gallate, a constituent of green tea, represses hepatic glucose production. J Biol Chem. 2002;277:34933–40.CrossRefPubMed Waltner-Law ME, Wang XL, Law BK, Hall RK, Nawano M, Granner DK. Epigallocatechin gallate, a constituent of green tea, represses hepatic glucose production. J Biol Chem. 2002;277:34933–40.CrossRefPubMed
7.
go back to reference Cheng J-T, Liu I-M. Stimulatory effect of caffeic acid on α1A-adrenoceptors to increase glucose uptake into cultured C2C12 cells. Naunyn Schmiedebergs Arch Pharmacol. 2000;362:122–7.CrossRefPubMed Cheng J-T, Liu I-M. Stimulatory effect of caffeic acid on α1A-adrenoceptors to increase glucose uptake into cultured C2C12 cells. Naunyn Schmiedebergs Arch Pharmacol. 2000;362:122–7.CrossRefPubMed
8.
go back to reference Ohno T, Kato N, Ishii C, Shimizu M, Ito Y, Tomono S, Kawazu S. Genistein augments cyclic adenosine 3’5’-monophosphate (cAMP) accumulation and insulin release in MIN6 cells. Endocr Res. 1993;19:273–85.CrossRefPubMed Ohno T, Kato N, Ishii C, Shimizu M, Ito Y, Tomono S, Kawazu S. Genistein augments cyclic adenosine 3’5’-monophosphate (cAMP) accumulation and insulin release in MIN6 cells. Endocr Res. 1993;19:273–85.CrossRefPubMed
9.
go back to reference Sarker MMR, Gohda E. Promotion of anti-keyhole limpet hemocyanin IgM and IgG antibody productions in vitro by red bell pepper extract. J Funct Foods. 2013;5:1918–26.CrossRef Sarker MMR, Gohda E. Promotion of anti-keyhole limpet hemocyanin IgM and IgG antibody productions in vitro by red bell pepper extract. J Funct Foods. 2013;5:1918–26.CrossRef
10.
go back to reference Goto T, Sarker MMR, Zhong M, Gohda E. Enhancement of immunoglobulin M production in B cells by the extract of Red bell pepper. J Health Sci. 2010;56:304–9.CrossRef Goto T, Sarker MMR, Zhong M, Gohda E. Enhancement of immunoglobulin M production in B cells by the extract of Red bell pepper. J Health Sci. 2010;56:304–9.CrossRef
11.
go back to reference Shah MA, Sarker MMR, Gousuddin M. Antidiabetic potential of Brassica Oleracea Var. Italica in type 2 diabetic sprague dawley (sd) rats. Int J Pharmacogn Phytochem Res. 2016;8:462–9. Shah MA, Sarker MMR, Gousuddin M. Antidiabetic potential of Brassica Oleracea Var. Italica in type 2 diabetic sprague dawley (sd) rats. Int J Pharmacogn Phytochem Res. 2016;8:462–9.
12.
go back to reference Sarker MMR, Mazumder MEH, Rashid MHO. In vitro Enhancement of Polyclonal IgM Production by Ethanolic Extract of Nigella sativa L. Seeds in whole Spleen Cells of Female BALB/c Mice. Bangladesh Pharm J. 2011;14:73–7. Sarker MMR, Mazumder MEH, Rashid MHO. In vitro Enhancement of Polyclonal IgM Production by Ethanolic Extract of Nigella sativa L. Seeds in whole Spleen Cells of Female BALB/c Mice. Bangladesh Pharm J. 2011;14:73–7.
13.
go back to reference Sarker MMR, Zihad MATR, Islam M, Nahar M, Islam MM, Imam H, Ghosh A, Mustapha MS, Ismail NE. Antihyperglycemic, insulin-sensitivity and antihyperlipidemic potential of Ganoderma lucidum, a dietary mushroom, on alloxan- and glucocorticoid-induced diabetic Long-Evans rats. Funct Foods Health Dis. 2015;5:450–66. Sarker MMR, Zihad MATR, Islam M, Nahar M, Islam MM, Imam H, Ghosh A, Mustapha MS, Ismail NE. Antihyperglycemic, insulin-sensitivity and antihyperlipidemic potential of Ganoderma lucidum, a dietary mushroom, on alloxan- and glucocorticoid-induced diabetic Long-Evans rats. Funct Foods Health Dis. 2015;5:450–66.
14.
go back to reference Lansky EP, Newman RA. < i > Punica granatum</i > (pomegranate) and its potential for prevention and treatment of inflammation and cancer. J Ethnopharmacol. 2007;109:177–206.CrossRefPubMed Lansky EP, Newman RA. < i > Punica granatum</i > (pomegranate) and its potential for prevention and treatment of inflammation and cancer. J Ethnopharmacol. 2007;109:177–206.CrossRefPubMed
15.
go back to reference Aviram M. Pomegranate juice as a major source for polyphenolic flavonoids and it is most potent antioxidant against LDL oxidation and atherosclerosis. Free Radic Res. 2002;36:71. Aviram M. Pomegranate juice as a major source for polyphenolic flavonoids and it is most potent antioxidant against LDL oxidation and atherosclerosis. Free Radic Res. 2002;36:71.
16.
go back to reference Su H-C, Hung L-M, Chen J-K. Resveratrol, a red wine antioxidant, possesses an insulin-like effect in streptozotocin-induced diabetic rats. Am J Phys Endocrinol Metab. 2006;290:E1339–46.CrossRef Su H-C, Hung L-M, Chen J-K. Resveratrol, a red wine antioxidant, possesses an insulin-like effect in streptozotocin-induced diabetic rats. Am J Phys Endocrinol Metab. 2006;290:E1339–46.CrossRef
17.
go back to reference Association AD. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2010;33:S62–9.CrossRef Association AD. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2010;33:S62–9.CrossRef
18.
go back to reference Faria A, Monteiro R, Mateus N, Azevedo I, Calhau C. Effect of pomegranate (Punica granatum) juice intake on hepatic oxidative stress. Eur J Nutr. 2007;46:271–8.CrossRefPubMed Faria A, Monteiro R, Mateus N, Azevedo I, Calhau C. Effect of pomegranate (Punica granatum) juice intake on hepatic oxidative stress. Eur J Nutr. 2007;46:271–8.CrossRefPubMed
19.
go back to reference Nekooeian AA, Eftekhari MH, Adibi S, Rajaeifard A. Effects of pomegranate seed Oil on insulin release in rats with type 2 diabetes. Iran J Med Sci. 2014;39:130.PubMedPubMedCentral Nekooeian AA, Eftekhari MH, Adibi S, Rajaeifard A. Effects of pomegranate seed Oil on insulin release in rats with type 2 diabetes. Iran J Med Sci. 2014;39:130.PubMedPubMedCentral
20.
go back to reference Masih M, Banerjee T, Banerjee B, Pal A. Antidiabetic activity of Acalypha indica linn. on normal and alloxan induced diabetic rats. Int J Pharm Pharm Sci. 2011;3:51–4. Masih M, Banerjee T, Banerjee B, Pal A. Antidiabetic activity of Acalypha indica linn. on normal and alloxan induced diabetic rats. Int J Pharm Pharm Sci. 2011;3:51–4.
21.
go back to reference Madkor HR, Mansour SW, Ramadan G. Modulatory effects of garlic, ginger, turmeric and their mixture on hyperglycaemia, dyslipidaemia and oxidative stress in streptozotocin–nicotinamide diabetic rats. Br J Nutr. 2011;105:1210–7.CrossRefPubMed Madkor HR, Mansour SW, Ramadan G. Modulatory effects of garlic, ginger, turmeric and their mixture on hyperglycaemia, dyslipidaemia and oxidative stress in streptozotocin–nicotinamide diabetic rats. Br J Nutr. 2011;105:1210–7.CrossRefPubMed
22.
go back to reference Bagri P, Ali M, Aeri V, Bhowmik M, Sultana S. Antidiabetic effect of < i > Punica granatum</i > flowers: Effect on hyperlipidemia, pancreatic cells lipid peroxidation and antioxidant enzymes in experimental diabetes. Food Chem Toxicol. 2009;47:50–4.CrossRefPubMed Bagri P, Ali M, Aeri V, Bhowmik M, Sultana S. Antidiabetic effect of < i > Punica granatum</i > flowers: Effect on hyperlipidemia, pancreatic cells lipid peroxidation and antioxidant enzymes in experimental diabetes. Food Chem Toxicol. 2009;47:50–4.CrossRefPubMed
23.
go back to reference Wu AH. Tietz clinical guide to laboratory tests. St. Louis: Saunders/Elsevier; 2006. Wu AH. Tietz clinical guide to laboratory tests. St. Louis: Saunders/Elsevier; 2006.
24.
go back to reference Korner J, Savontaus E, Chua S, Leibel R, Wardlaw S. Leptin regulation of Agrp and Npy mRNA in the rat hypothalamus. J Neuroendocrinol. 2001;13:959–66.CrossRefPubMed Korner J, Savontaus E, Chua S, Leibel R, Wardlaw S. Leptin regulation of Agrp and Npy mRNA in the rat hypothalamus. J Neuroendocrinol. 2001;13:959–66.CrossRefPubMed
25.
go back to reference Sugiuchi H, Uji Y, Okabe H, Irie T, Uekama K, Kayahara N, Miyauchi K. Direct measurement of high-density lipoprotein cholesterol in serum with polyethylene glycol-modified enzymes and sulfated alpha-cyclodextrin. Clin Chem. 1995;41:717–23.PubMed Sugiuchi H, Uji Y, Okabe H, Irie T, Uekama K, Kayahara N, Miyauchi K. Direct measurement of high-density lipoprotein cholesterol in serum with polyethylene glycol-modified enzymes and sulfated alpha-cyclodextrin. Clin Chem. 1995;41:717–23.PubMed
26.
go back to reference Jelodar G, Mohsen M, Shahram S. Effect of walnut leaf, coriander and pomegranate on blood glucose and histopathology of pancreas of alloxan induced diabetic rats. Afr J Tradit Complement Altern Med. 2008;4:299–305.CrossRef Jelodar G, Mohsen M, Shahram S. Effect of walnut leaf, coriander and pomegranate on blood glucose and histopathology of pancreas of alloxan induced diabetic rats. Afr J Tradit Complement Altern Med. 2008;4:299–305.CrossRef
27.
go back to reference Blois MS. Antioxidant determinations by the use of a stable free radical. Nature. 1958;181:1199–200.CrossRef Blois MS. Antioxidant determinations by the use of a stable free radical. Nature. 1958;181:1199–200.CrossRef
28.
go back to reference Papaccio G, Pisanti FA, Latronico MV, Ammendola E, Galdieri M. Multiple low-dose and single high-dose treatments with streptozotocin do not generate nitric oxide. J Cell Biochem. 2000;77:82–91.CrossRefPubMed Papaccio G, Pisanti FA, Latronico MV, Ammendola E, Galdieri M. Multiple low-dose and single high-dose treatments with streptozotocin do not generate nitric oxide. J Cell Biochem. 2000;77:82–91.CrossRefPubMed
29.
go back to reference Vattem D, Shetty K. Biological functionality of ellagic acid: a review. J Food Biochem. 2005;29:234–66.CrossRef Vattem D, Shetty K. Biological functionality of ellagic acid: a review. J Food Biochem. 2005;29:234–66.CrossRef
30.
go back to reference Kern PA, Ranganathan S, Li C, Wood L, Ranganathan G. Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance. Am J Phys Endocrinol Metab. 2001;280:E745–51. Kern PA, Ranganathan S, Li C, Wood L, Ranganathan G. Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance. Am J Phys Endocrinol Metab. 2001;280:E745–51.
31.
go back to reference Arnalich F, Hernanz A, Lopez-Maderuelo D, Pena J, Camacho J, Madero R, Vazquez J, Montiel C. Enhanced acute-phase response and oxidative stress in older adults with type II diabetes. Horm Metab Res. 2000;32:407–12.CrossRefPubMed Arnalich F, Hernanz A, Lopez-Maderuelo D, Pena J, Camacho J, Madero R, Vazquez J, Montiel C. Enhanced acute-phase response and oxidative stress in older adults with type II diabetes. Horm Metab Res. 2000;32:407–12.CrossRefPubMed
32.
go back to reference Guha M, Bai W, Nadler JL, Natarajan R. Molecular mechanisms of tumor necrosis factor α gene expression in monocytic cells via hyperglycemia-induced oxidant stress-dependent and-independent pathways. J Biol Chem. 2000;275:17728–39.CrossRefPubMed Guha M, Bai W, Nadler JL, Natarajan R. Molecular mechanisms of tumor necrosis factor α gene expression in monocytic cells via hyperglycemia-induced oxidant stress-dependent and-independent pathways. J Biol Chem. 2000;275:17728–39.CrossRefPubMed
34.
go back to reference Shukla M, Gupta K, Rasheed Z, Khan KA, Haqqi TM. Consumption of hydrolyzable tannins-rich pomegranate extract suppresses inflammation and joint damage in rheumatoid arthritis. Nutrition. 2008;24:733–43.CrossRefPubMedPubMedCentral Shukla M, Gupta K, Rasheed Z, Khan KA, Haqqi TM. Consumption of hydrolyzable tannins-rich pomegranate extract suppresses inflammation and joint damage in rheumatoid arthritis. Nutrition. 2008;24:733–43.CrossRefPubMedPubMedCentral
35.
go back to reference Esmaillzadeh A, Tahbaz F, Gaieni I, Alavi-Majd H, Azadbakht L. Concentrated pomegranate juice improves lipid profiles in diabetic patients with hyperlipidemia. J Med Food. 2004;7:305–8.CrossRefPubMed Esmaillzadeh A, Tahbaz F, Gaieni I, Alavi-Majd H, Azadbakht L. Concentrated pomegranate juice improves lipid profiles in diabetic patients with hyperlipidemia. J Med Food. 2004;7:305–8.CrossRefPubMed
36.
go back to reference Aviram M, Dornfeld L, Kaplan M, Coleman R, Gaitini D, Nitecki S, Hofman A, Rosenblat M, Volkova N, Presser D. Pomegranate juice flavonoids inhibit low-density lipoprotein oxidation and cardiovascular diseases: studies in atherosclerotic mice and in humans. Drugs Exp Clin Res. 2001;28:49–62. Aviram M, Dornfeld L, Kaplan M, Coleman R, Gaitini D, Nitecki S, Hofman A, Rosenblat M, Volkova N, Presser D. Pomegranate juice flavonoids inhibit low-density lipoprotein oxidation and cardiovascular diseases: studies in atherosclerotic mice and in humans. Drugs Exp Clin Res. 2001;28:49–62.
37.
go back to reference Pari L, Latha M. Effect of Cassia auriculata flowers on blood sugar levels, serum and tissue lipids in streptozotocin diabetic rats. Singapore Med J. 2002;43:617–21.PubMed Pari L, Latha M. Effect of Cassia auriculata flowers on blood sugar levels, serum and tissue lipids in streptozotocin diabetic rats. Singapore Med J. 2002;43:617–21.PubMed
38.
go back to reference Rosenblat M, Hayek T, Aviram M. Anti-oxidative effects of pomegranate juice (PJ) consumption by diabetic patients on serum and on macrophages. Atherosclerosis. 2006;187:363–71.CrossRefPubMed Rosenblat M, Hayek T, Aviram M. Anti-oxidative effects of pomegranate juice (PJ) consumption by diabetic patients on serum and on macrophages. Atherosclerosis. 2006;187:363–71.CrossRefPubMed
39.
go back to reference Kurowska E, Borradaile N, Spence J, Carroll K. Hypocholesterolemic effects of dietary citrus juices in rabbits. Nutr Res. 2000;20:121–9.CrossRef Kurowska E, Borradaile N, Spence J, Carroll K. Hypocholesterolemic effects of dietary citrus juices in rabbits. Nutr Res. 2000;20:121–9.CrossRef
40.
go back to reference Koba K, Akahoshi A, Yamasaki M, Tanaka K, Yamada K, Iwata T, Kamegai T, Tsutsumi K, Sugano M. Dietary conjugated linolenic acid in relation to CLA differently modifies body fat mass and serum and liver lipid levels in rats. Lipids. 2002;37:343–50.CrossRefPubMed Koba K, Akahoshi A, Yamasaki M, Tanaka K, Yamada K, Iwata T, Kamegai T, Tsutsumi K, Sugano M. Dietary conjugated linolenic acid in relation to CLA differently modifies body fat mass and serum and liver lipid levels in rats. Lipids. 2002;37:343–50.CrossRefPubMed
Metadata
Title
The effect of pomegranate fresh juice versus pomegranate seed powder on metabolic indices, lipid profile, inflammatory biomarkers, and the histopathology of pancreatic islets of Langerhans in streptozotocin-nicotinamide induced type 2 diabetic Sprague–Dawley rats
Authors
Seyedeh Zeinab Taheri Rouhi
Md. Moklesur Rahman Sarker
Asmah Rahmat
Saad Ahmed Alkahtani
Fauziah Othman
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Complementary Medicine and Therapies / Issue 1/2017
Electronic ISSN: 2662-7671
DOI
https://doi.org/10.1186/s12906-017-1667-6

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