Anti-Obesity and Antihyperglycemic Effects of Crataegus aronia Extracts: In Vitro and in Vivo Evaluations

DOI: 10.4236/fns.2013.49126   PDF   HTML     4,247 Downloads   6,675 Views   Citations

Abstract

Hypocholesterolemic activity of Crataegus aronia L. (Rosaceae) is therapeutically praised. Its potent antiobesity (P < 0.001, n = 6 - 8) as well as marked triacylglycerol-reducing efficacies (P < 0.001, n = 6 - 8) in 10 weeks-high cholesterol diet (HCD) fed rats are demonstrated. Pancreatic triacylglycerol lipase (PL), α-amylase and α-glucosidase are an interesting pharmacological target for the management of dyslipidemia, atherosclerosis, diabetes and obesity. Comparable to acarbose, acute starch induced postprandial hyperglycaemia as well glycemic excursions in normoglycemic overnight fasting rats was highly significantly (P < 0.001) dampened by C. aronia 100, 200 and 400 mg/Kg b.wt aqueous extracts (AE), but not acute glucose evoked postprandial hyperglycaemia increments, unlike diabetes pharmaco-therapeutics metformin and glipizide. C. aronia aerial parts as well as fruits AEs (0.1 - 10 mg/mL) were identified as in vitro dual inhibitors of α-amylase and α-glucosidase with respective IC50 (mg/mL) of 2.1 ± 0.3 and 3.5 ± 0.7. Still, it lacked on in vitro hindrance of glucose movement, dissimilar to guar gum. Equivalent to orlistat (PL IC50 of 0.1 ± 0.0 μg/mL), C. aronia tested AEs and its purified bioactive phytoconstituents; quercetin and rutin, inhibited highly substantially in a dose dependent trend PL in vitro (n = 3), in an ascending order of obtained PL-IC50 (μg/mL): quercetin; 30.1 ± 2.8, rutin; 77.3 ± 11.7, C. aronia aerial parts; 225.2 ± 33.4 and C. aronia fruits; 286.1 ± 37.4. Flavonoid-rich C. aronia, as a functional food and a nutraceutical, modulating gastrointestinal carbohydrate and lipid digestion and absorption, maybe be advocated as an exquisite and potential candidate for combinatorial obesity-diabetes prevention and phytotherapy.

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E. Al-Hallaq, V. Kasabri, S. Abdalla, Y. Bustanji and F. Afifi, "Anti-Obesity and Antihyperglycemic Effects of Crataegus aronia Extracts: In Vitro and in Vivo Evaluations," Food and Nutrition Sciences, Vol. 4 No. 9, 2013, pp. 972-983. doi: 10.4236/fns.2013.49126.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] K. Ajlouni, Y. S. Khader, A. Batieha, H. Ajloun and M. El-Khateeb, “An Increase of Diabetes Mellitus in Jordan over 10 Years,” Journal of Diabetes Complications, Vol. 22, No. 5, 2008, pp. 317-324.
[2] N. R. Bulatova, A. F. Yousef and S. M. AbuRuz, “Anti platelet Therapy for Primary and Secondary Prevention in Jordanian Patients with Diabetes Mellitus,” Thrombosis Research, Vol. 121, No. 1, 2007, pp. 43-50. doi:10.1016/j.thromres.2007.03.006
[3] M. Zindah, A. Belbeisi, H. Walke and A. H. Mokdad, “Obesity and Diabetes in Jordan: Findings from the Be havioural Risk Factor Surveillance System, 2004,” Pre vention of Chronic Disease, Vol. 5, No. 1, 2008, pp. 1-8.
[4] International Diabetes Federation (IDF), “Prevalence Estimates of Diabetes Mellitus (DM)-MENA,” IDF Dia betes Atlas, 4th Edition, 2009. http://www.diabetesatlas.org/content/prevalence-estimates-diabetes-mellitus-dm-2010
[5] Z. H. Israili, “Advances in the Treatment of Type 2 Dia betes Mellitus,” American Journal of Therapeutics, Vol. 18, No. 2, 2011, pp. 117-152. doi:10.1097/MJT.0b013e3181afbf51
[6] F. U. Afifi-Yazar, V. Kasabri and R. Abu Dahab, “Me dicinal Plants from Jordan in the Treatment of Diabetes: Traditional Uses vs. in Vitro and in Vivo Evaluations. Mini-Review,” Planta Medica, Vol. 77, No. 11, 2011, pp. 1210-1220. doi:10.1055/s-0031-1279983
[7] C. Anderson, S. Rayalam, M. A. Della-Fera and C. A. Baile, “Phytochemicals and Adipogenesis,” Biofactors, Vol. 36, No. 6, 2010, pp. 415-422. doi:10.1002/biof.115
[8] M. Kazemipoor, C. W. W. M. Radzi, G. A. Cordell and I. Yaze, “Potential of Traditional Medicinal Plants for Treat ing Obesity: A Review,” 2010 International Conference on Nutrition and Food Sciences. IPCBEE, Singapore, Vol. 39, No. 1, 2012, pp. 1-6.
[9] WHO, “Obesity and Overweight 2012,” 2012. http://www.who.int/mediacentre/factsheets/fs311/en/
[10] J. W. Yun, “Possible Antiobesity Therapeutics from Na ture—A Review,” Phytochemistry, Vol. 71, No. 14-15, 2010, pp. 1625-1641. doi:10.1016/j.phytochem.2010.07.011
[11] A. Al-Aboudi and F. U. Afifi, “Plants Used for the Treat ment of Diabetes in Jordan: A Review of Scientific Evi dence,” Pharmaceutical. Biology, Vol. 49, No. 3, 2011, pp. 221-239. doi:10.3109/13880209
.2010.501802
[12] M. Wazaify, F. U. Afifi, M. El-Khateeb and K. Ajlouni, “Complementary and Alternative Medicine Use among Jordanian Diabetes Patients,” Complementary Therapies in Clinical Practice, Vol. 17, No. 2, 2011, pp. 71-75. doi:10.1016/j.ctcp.2011.02.002
[13] E. K. Al-Hallaq, F. U. Afifi and S. S. Abdalla, “Evalua tion of the Hypocholesterolemic Effect and Phytochemi cal Screening of the Hydroethanolic Extract of Crataegus aronia from Jordan,” Natural Product Communications, Vol. 7, No. 1, 2012, pp. 35-38.
[14] R. Bahri-Sahloul, S. Ammar, R. B. Fredj, S. Saguem, S. Grec, F. Trotin and F. H. Skhiri, “Polyphenol Contents and Antioxidant Activities of Extracts from Flowers of Two Crataegus azarolus L. Varieties,” Pakistan Journal of Biological Sciences, Vol. 12, No. 9, 2009, pp. 660-668. doi:10.3923/pjbs.
2009.660.668
[15] O. Caliskan, K. Gündüz, S. Serce, C. Toplu, O. Kami loglu, M. Sengül and S. Ercisli, “Phytochemical Charac terization of Several Hawthorn (Crataegus spp.) Species Sampled from the Eastern Mediterranean Region of Tur key,” Pharmacognosy Magazine, Vol. 8, No. 29, 2012, pp. 16-21. doi:10.4103/0973-1296.93305
[16] N. Keskin, R. Mammadov and P. Ili, “The Effects of Crataegus aronia var. dentata Browicz Extract on Bio chemical Indices and Apoptosis in Partially Hepatec tomized Liver in Rats,” Bosnian Journal of Basic Medical Sciences, Vol. 12, No. 3, 2012, pp. 177-181.
[17] R. Khalil, N. Abuharfeil and B. Shabsoug, “The Effect of Crataegus aronia Aqueous Extract in Rabbits Fed with High Cholesterol Diet,” European Journal of Scientific Research, Vol. 22, 2008, pp. 352-360.
[18] D. Kumar, V. Arya, Z. A. Bhat, N. A. Khan and D. N. Prasad, “The Genus Crataegus: Chemical and Pharma cological Perspectives,” Brazilian Journal of Pharmcog nosy, Vol. 22, No. 5, 2012, pp. 1187-1200.
[19] P. Ljubuncic, I. Portnaya, U. Cogan, H. Azaizeh and A. Bomzon, “Antioxidant Activity of Crataegus aronia Aqueous Extract Used in Traditional Arab Medicine in Israel,” Journal of Ethnopharmacology, Vol. 101, No. 1-3, 2005, pp. 153-161. doi:10.1016/j.jep.2005.04.024
[20] P. Ljubuncic, H. Azaizeh, U. Cogan and A. Bomzon, “The Effects of a Decoction Prepared from the Leaves and Unripe Fruits of Crataegus aronia in Streptozotocin Induced Diabetic Rats,” Journal of Complementary and Integrative Medicine, Vol. 3, No. 1, 2006, in press. doi:10.2202/1553-3840.1027
[21] A. S. Shatoor, “Acute and Sub-Acute Toxicity of Cratae gus aronia syn. azarolus (L.) Whole Plant Aqueous Ex tract in Wistar Rats,” American Journal of Pharmacology and Toxicology, Vol. 6, No. 2, 2011, pp. 37-45. doi:10.3844/ajptsp.2011.37.45
[22] A. S. Shatoor, “Cardio-Tonic Effect of the Aqueous Ex tract of Whole Plant of Crataegus aronia syn: azarolus (L) on Isolated Rabbit’s Heart,” African Journal of Pharmacy and Pharmacology, Vol. 6, No. 26, 2012, pp. 1901-1909.
[23] A. S. Shatoor, H. Soliman, F. Al-Hashem, B. E. Gamal, A. Othman and N. El-Menshawy, “Effect of Hawthorn (Cra taegus aronia syn. azarolus (L)) on Platelet Function in Albino Wistar Rats,” Thrombosis Research, Vol. 130, No. 1, 2012, pp. 75-80.
[24] M. S. Shekha and O. A. M. AlHabib, “Vasorelaxant, An tispasmodic and Cardiotonic Effect of the Chloform Frac tion of Crataegus aronia on Isolated Rat Muscles,” In ternational Journal of Biological and Biomedical Sci ences, Vol. 1, No. 1, 2012, pp. 6-11.
[25] M. C. Tassell, R. Kingston, D. Gilroy, M. Lehane and A. Furey, “Hawthorn (Crataegus spp.) in the Treatment of Cardiovascular Disease,” Pharmacognosy Reviews, Vol. 4, No. 7, 2010, pp. 32-41.
doi:10.4103/0973-7847.65324
[26] S. Adisakwattana and B. Chanathong, “Alpha-Glucosi dase Inhibitory Activity and Lipid-Lowering Mechanisms of Moringa oleifera Leaf Extract,” European Review for Medical and Pharmacological Sciences, Vol. 15, No. 7, 2011, pp. 803-808.
[27] C. B. Etoundi, D. Kuate, J. L. Ngondi and J. Oben, “Anti Amylase, Antilipase and Antioxidant Effects of Aqueous Extracts of Some Cameroonian Spices,” Journal of Natu ral Products, Vol. 3, 2010, pp. 165-171.
[28] I. Gurbuz, O. Ustun, E. Yesilada, E. Sezik and O. Kutsal, “Anti-Ulcerogenic Activity of Some Plants Used as Folk Remedy in Turkey,” Journal of Ethnopharmacology, Vol. 88, No. 1, 2003, pp. 93-97. doi:10.1016/S0378-8741(03)00174-0
[29] S. Habtemariam, “The Antiobesity Potential of Sigmoidin A,” Pharmaceutical Biology, Vol. 50, No. 12, 2012, pp. 1519-1522. doi:10.3109/13880209.2012.688838
[30] Y. Bustanji, I. AlMasri, M. Mohammad, M. Hudaib, K. Tawaha, H. Tarazi and H. AlKhatib, “Pancreatic Lipase Inhibition Activities of Trilactone Terpenes of Ginkgo biloba,” Journal of Enzyme Inhibition and Medicinal Chemistry, Vol. 26, No. 4, 2011, pp. 453-459. doi:10.3109/14756366.2010.525509
[31] V. Kasabri, F. U. Afifi and I. Hamdan, “In Vitro and in Vivo Antihyperglycemic Effects of Five Selected Indige nous Plants from Jordan Used in Traditional Medicine,” Journal of Ethnopharmacology, Vol. 133, No. 2, 2011, pp. 888-896. doi:10.1016/j.jep.2010.11.025
[32] V. Kasabri, R. Abu-Dahab, F. U. Afifi, R. Naffa and L. Majdalawi, “Modulation of Pancreatic MIN6 Insulin Se cretion and Proliferation and Extrapancreatic Glucose Ab sorption with Achillea santolina, Eryngium creticum and Pistacia atlantica Extracts: In vitro Evaluation,” Journal of Experimental Integrative Medicine, Vol. 2, No. 3, 2012, pp. 245-254.
[33] M. S. Butt, A. Ahmad and M. K. Sharif, “Influence of Pectin and Guar Gum Composite Flour on Plasma Bio chemical Profile of Streptozocin-Induced Diabetic Male Albino Rats,” International Journal of Food Properties, Vol. 10, No. 2, 2007, pp. 345-361. doi:10.1080/10942910601052707
[34] A. M. Gallagher, P. R. Flatt, G. Duggy and Y. H. A. Ab del-Wahab, “The Effects of Traditional Antidiabetic Plants on in Vitro Glucose Diffusion,” Nutrition Research, Vol. 23, No. 3, 2003, pp. 413-424. doi:10.1016/S0271-5317(02)00533-X
[35] S. Y. Pan, R. Yang, H. Dong, Z. L. Yu and K. M. Ko, “Bifendate Treatment Attenuates Hepatic Steatosis in Cholesterol/Bile Salt and High-Fat Diet Induced Hyper cholesterolemia in Mice,” European Journal of Pharma cology, Vol. 552, No. 1-3, 2006, pp. 170-175. doi:10.1016/j.ejphar.2006.09.011
[36] C. D. Zheng, Y. Q. Duan, J. M. Gao and Z. G. Ruan, “Screening for Anti-Lipase Properties of 37 Traditional Chinese Medicinal Herbs,” Journal of the Chinese Medi cal Association, Vol. 73, No. 6, 2010, pp. 319-324. doi:10.1016/S1726-4901(10)70068-X
[37] C. Fan, J. Yan, Y. Qian, X. Wo and L. Gao, “Regulation of Lipoprotein Lipase Expression by Effects of Hawthorn Flavonoids on Peroxisome Proliferator Response Element Pathway,” Journal of Pharmaceutical Sciences, Vol. 100, No. 1, 2006, pp. 51-58. doi:10.1254/jphs.FP0050748
[38] T. Jurikova, J. Sochor, O. Rop, J. Mlcek, S. Balla, L. Szekeres, V. Adam and R. Kizek, “Polyphenolic Profile and Biological Activity of Chinese Hawthorn (Crataegus pinnatifida BUNGE) Fruits,” Molecules, Vol. 17, No. 12, 2012, pp. 14490-14509. doi:10.3390/molecules171214490
[39] S. Kausar, Z. Zaheer, M. Saqib and B. Zia, “The Effect of Crataegus (Hawthorn) Extract Alone and in Combination with Simvastatin on Serum Lipid Profile in Hyperlipi demic Albino Rats,” Biomedica, Vol. 27, 2011, pp. 140-147.
[40] A. L. De le Garza, F. I. Milagro, N. Boque, J. Campion and J. A. Martinez, “Natural Inhibitors of Pancreatic Li pase as New Players in Obesity Treatment,” Planta Medica, Vol. 77, No. 8, 2011, pp. 773-785. doi:10.1055/s-0030-1270924
[41] Z. Zhang, W. K. K. Ho, Y. Huang, A. E. James, L. W. Lam and Z. Y. Chen, “Hawthorn Fruit Is Hypolipidemic in Rabbits Fed a High Cholesterol Diet,” Journal of Nutrition, Vol. 132, No. 1, 2002, pp. 5-10.
[42] W. Huang, X. Ye, Z. Zhao, P. Lan, L. Wang, M. Liu, Y. Gao, J. Zhu, P. Li and P. Feng, “The Inhibition Activity of Chemical Constituents in Hawthorn Fruit and Their Synergistic Action to HMG-CoA Reductase,” Zhongguo Zhong Yao Za Zhi, Vol. 35, No. 18, 2010, pp. 2428-2431.
[43] Y. Guo, G. Wu, X. Su, H. Yang and J. Zhang, “Antiobe sity Action of a Daidzein Derivative on Male Obese Mice Induced by a High Fat Diet,” Nutrition Research, Vol. 29, No. 9, 2009, pp. 656-663. doi:10.1016/j.nutres.2009.09.005
[44] M. H. Moon, J. K. Jeong, Y. J. Lee, J. W. Seol, D. C. Ahn, I. S. Kim and S. Y. Park, “18β-Glycyrrhetinic Acid Inhi bits Adipogenic Differentiation and Stimulates Lipoly sis,” Biochemical and Biophysical Research Communi cations, Vol. 420, 2012, pp. 805-810. doi:10.1016/j.bbrc.2012.03.078
[45] A. Bryson, S. de la Motte and C. Dunk, “Reduction of Dietary Fat Absorption by the Novel Gastrointestinal Li pase Inhibitor Cetilistat in Healthy Volunteers,” British Journal of Clinical Pharmacology, Vol. 67, No. 3, 2009, pp. 309-315. doi:10.1111/j.1365-2125.2008.03311.x
[46] S. Ebdrup, H. H. Refsgaard, C. Fledelius and P. Jacobsen, “Synthesis and Structure-Activity Relationship for a Novel Class of Potent and Selective Carbamate-Based In hibitors of Hormone Selective Lipase with Acute in Vivo Antilipolytic Effects,” Journal of Medicinal Chemistry, Vol. 50, No. 22, 2007, pp. 5449-5456. doi:10.1021/jm0607653
[47] J. Zhang, M. J. Kang, M. J. Kim, M. E. Kim, M. E. Song, J. H. Song, Y. M. Lee and J. I. Kim, “Pancreatic Lipase Inhibitory Activity of Taraxacum officinale in Vitro and in Vivo,’’ Nutrition Research and Practice, Vol. 2, No. 4, 2008, pp. 200-203. doi:10.4162/nrp.2008.2.4.200
[48] A. S. Wierzbicki, T. C. Hardman and A. Viljoen, “New Lipid-Lowering Drugs: An Update,” International Jour nal of Clinical Practice, Vol. 66, No. 3, 2012, pp. 270-280. doi:10.1111/j.1742-1241.2011.02867.x
[49] H. Li, F. Song, J. Xing, R. Tsao, R. Liu and S. Liu, “Screening and Structural Characterization of α-Gluco sidase Inhibitors from Hawthorn Leaf Flavonoids Extract by Ultrafiltration LC-DAD-MSn and SORI-CID FTICR MS,” Journal of American Society for Mass Spectrome try, Vol. 20, No. 8, 2009, pp.1496-1503. doi:10.1016/j.jasms.2009.04.003
[50] P. Fan, L. Terrier, A. E. Hay, A. Marston and K. Hos tettmann, “Antioxidant and Enzyme Inhibition Activities and Chemical Profiles of Polygonum sachalinensis F. Schmidt ex Maxim (Polygonaceae),” Fitoterapia, Vol. 81, No. 2, 2010, pp. 124-131. doi:10.1016/j.fitote.2009.08.019
[51] Y. Q. Li, F. C. Zhou, F. Gao, J. S. Bian and F. Shan, “Comparative Evaluation of Quercetin, Isoquercetin and Rutin as Inhibitors of Alpha-Glucosidase,” Journal of Agriculture and Food Chemistry, Vol. 57, No. 24, 2009, pp. 11463-11468. doi:10.1021/jf903083h
[52] P. Bansal, P. Paul, G. Shankar, D. Munjal, P. G. Nayak, K. I. Priyadarsini and M. K. Unnikrishnan, “Flavonoid Rich Fraction of Pilea microphylla (L.) Attenuates Meta bolic Abnormalities and Improves Pancreatic Function in C57BL/KsJ-db-db Mice,” Biomedicine and Preventive Nutrition, Vol. 1, No. 4, 2011, pp. 268-272. doi:10.1016/j.bionut.2011.09.002
[53] S. Adisakwattana, O. Lerdsuwankij, U. Poputtachai, A. Minipun and C. Suparpprom, “Inhibitory Activity of Cin namon Bark Species and Their Combination Effect with Acarbose against Intestinal α-Glucosidase and Pancreatic α-Amylase,” Plant Foods and Human Nutrition, Vol. 66, No. 2, 2011, pp. 143-148. doi:10.1007/s11130-011-0226-4
[54] D. Grussu, D. Stewart and G. J. McDoagall, “Berry Polyphenols Inhibit α-Amylase in Vitro: Identifying Ac tive Components in Rowanberry and Raspberry,” Journal of Agriculture and Food Chemistry, Vol. 59, No. 6, 2011, pp. 2324-2331. doi:10.1021/jf1045359
[55] J. Maolly, K. Gurney, K. Shan, P. Yan and S. Chen, “In creased Variability and Abnormalities in Pancreatic En zyme Concentrations in otherwise Asymptomatic Sub jects with Type 2 Diabetes,” Diabetes Metabolic Syn drome and Obesity: Targets and Therapy, Vol. 5, 2012, pp. 419-429.
[56] N. Ikarashi, R. Takeda, K. Ito, W. Ochiai and K. Sugi yama, “The Inhibition of Lipase and Glucosidase Activi ties by Acacia Polyphenol,” Evidence-Based Comple mentary and Alternative Medicine, Vol. 2011, 2011, Arti cle ID: 272075. doi:10.1093/ecam/neq043
[57] S. N. Raju, D. S. Kumar, D. Banji, A. Harani, P. Shankar, P. A. Kumar and V. R. Reddy, “Inhibitory Effects of Ethanolic Extract of Piper trioicum on Amylase, Lipase and α-Glucosidase,” Der Pharmacia Lettre Journal, Vol. 2, 2010, pp. 237-244.
[58] M. I. Kotowaroo, M. F. Mahomoodally, A. Gurib-Fakim and A. H. Subratty, “Screening of Traditional Antidia betic Medicinal Plants of Mauritius for Possible α-Amy lase Inhibitory Effects in Vitro,” Phytotherapy Research, Vol. 20, No. 3, 2006, pp. 228-231. doi:10.1002/ptr.1839
[59] W. C. Obiro, T. Zhang and B. Jiang, “The Nutraceutical Role of the Phaseolus vulgaris α-Amylase Inhibitor,” British Journal of Nutrition, Vol. 100, No. 1, 2008, pp. 1 12.
doi:10.1017/S0007114508879135
[60] X. Wu, X. Xu, J. Shen, N. V. Perricone and H. G. Preuss, “Enhanced Weight Loss from a Dietary Supplement Con taining Standardized Phaseolus vulgaris Extract in Overweight Man and Women,” Journal of Applied Re search, Vol. 10, No. 2, 2010, pp. 73-79.
[61] A. Gholamhoseinian, B. Shahouzehi and F. Sharifi-far, “Inhibitory Effect of Some Plant Extracts on Pancreatic Lipase,” International Journal of Pharmacology, Vol. 6, No. 1, 2010, pp. 18-24.
doi:10.3923/ijp.2010.18.24
[62] R. H. Eckel and R. M. Krauss, “American Heart Associa tion Call to Action: Obesity as a Major Risk Factor for Coronary Heart Disease,” Circulation, Vol. 978, 1998, pp. 2099-2100.
doi:10.1161/01.CIR.97.21.2099
[63] B. L. McVeigh, B. L. Dillingham, J. W. Lampe and A. M. Duncan, “Effect of Soy Protein Varying in Isoflavone Content on Serum Lipids in Healthy Young Men,” Ameri can Journal of Clinical Nutrition, Vol. 83, No. 2, 2006, pp. 244-251.
[64] K. Mnafgui, K. Hamden, H. Ben Salah, M. Kchaou, M. Nasri, S. Slama, F. Derbali, N. Allouche and A. Elfeki, “Inhibitory Activities of Zygophyllum album: A Natural Weight-Lowering Plant on Key Enzymes in High-Fat Diet Fed Rats,” Evidence Based Complementary Alterna tive Medicine, Vol. 2012, 2012, Article ID: 620384.
[65] S. M. Jeong, M. J. Kang, H. N. Choi, J. H. Kim and J. I. Kim, “Quercetin Ameliorates Hyperglycemia and Disli pidemia and Improves Antioxidant Status in Type 2 Dia betic db/db Mice,” Nutrition Research and Practice, Vol. 6, No. 3, 2012, pp. 201-207.

  
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