Nutrition Research and Practice

The Korean Nutrition Society (한국영양학회)
권호 표지
DOI QR코드

DOI QR Code

The effects of pomegranate peel added bread on anthropometric measurements, metabolic and oxidative parameters in individuals with type 2 diabetes: a double-blind, randomized, placebo-controlled study

  • Received : 2022.09.14
  • Accepted : 2023.02.08
  • Published : 2023.08.01
Download PDF
⟨ Previous Next ⟩

Abstract

BACKGROUND/OBJECTIVES: The aim of this study was to evaluate the sensory properties of antioxidant-rich bread made by adding pomegranate peels and their effects on anthropometric measurements and metabolic and oxidative parameters of individuals with type 2 diabetes after consumption. SUBJECTS/METHODS: This randomized, double-blind, placebo-controlled study was conducted with 22 individuals aged between 19 and 64 years who had been diagnosed with type 2 diabetes for at least 5 years, used only metformin, did not lose more than 10% of their body weight in the last 6 months, and had a body mass index of ≥ 25.0 kg/m2. While the study group (n = 11) consumed bread containing 500 mg pomegranate peel daily for 8 wk, the control group (n = 11) consumed standard bread. Anthropometric measurements and metabolic and oxidative parameters of individuals were evaluated at the beginning and end of the study. RESULTS: Decreases were detected in the waist circumference, waist/hip and waist/height ratios, body fat percentages, blood pressure, and serum insulin, triglyceride, and total cholesterol levels in the individuals in the treatment group, compared with those in the control group (P < 0.05). CONCLUSIONS: Pomegranate peel consumption by individuals with type 2 diabetes may have positive effects on anthropometric measurements and glycemic and lipid parameters.

Keywords

Acknowledgement

We would like to thank all the individuals for their cooperation who participated in our study.

References

  1. International Diabetes Federation. IDF Diabetes Atlas 10th Edition 2021 [Internet]. Brussels: IDF; 2021 [cited 2022 April 10]. Available from: https://idf.org/e-library/epidemiology-research/diabetes-atlas.html. 
  2. Banihani S, Swedan S, Alguraan Z. Pomegranate and type 2 diabetes. Nutr Res 2013;33:341-8.  https://doi.org/10.1016/j.nutres.2013.03.003
  3. Lewis GF, Carpentier A, Adeli K, Giacca A. Disordered fat storage and mobilization in the pathogenesis of insulin resistance and type 2 diabetes. Endocr Rev 2002;23:201-29.  https://doi.org/10.1210/edrv.23.2.0461
  4. Kyrou I, Tsigos C. Obesity in the elderly diabetic patient: is weight loss beneficial? Diabetes Care 2009;32 Suppl 2:S403-9.  https://doi.org/10.2337/dc09-S348
  5. Williams K, Tchernof A, Hunt KJ, Wagenknecht LE, Haffner SM, Sniderman AD. Diabetes, abdominal adiposty, and atherogenic dislipoproteinemia in women compared with men. Diabetes 2008;57:3289-96.  https://doi.org/10.2337/db08-0787
  6. Parhofer KG. Interaction between glucose and lipid metabolism: more than diabetic dyslipidemia. Diabetes Metab J 2015;39:353-62.  https://doi.org/10.4093/dmj.2015.39.5.353
  7. Preedy RV. Diabetes: Oxidative stress and dietary antioxidants. In: Preddy VR, editor. Diabetes: Oxidative Stress and Dietary Antioxidants. London: Academic Press; 2020. p.36-41. 
  8. Green M, Arora K, Prakash S. Microbial Medicine: Prebiotic and probiotic functional foods to target obesity and metabolic syndrome. Int J Mol Sci 2020;21:2890. 
  9. Grabez M, Skrbic R, Stojiljkovic MP, Rudic-Grujic V, Paunovic M, Arsic A, Petrovic S, Vucic V, Mirjanic-Azaric B, Savikin K, et al. Beneficial effects of pomegranate peel extract on plasma lipid profile, fatty acids levels and blood pressure in patients with diabetes mellitus type-2: a randomized, double-blind, placebocontrolled study. J Funct Foods 2020;64:103692. 
  10. Viuda-Martos M, Fernandez-Lopez J, Perez-Alvarez JA. Pomegranate and its many functional components as related to human health: a review. Compr Rev Food Sci Food Saf 2010;9:635-54.  https://doi.org/10.1111/j.1541-4337.2010.00131.x
  11. Cam M, Icyer NC, Erdogan F. Pomegranate peel phenolics: Microencapsulation, storage stability and potential ingredient for functional food development. Lebensm Wiss Technol 2014;55:117-23.  https://doi.org/10.1016/j.lwt.2013.09.011
  12. Akhtar S, Ismail T, Fraternale D, Sestili P. Pomegranate peel and peel extracts: chemistry and food features. Food Chem 2015;174:417-25.  https://doi.org/10.1016/j.foodchem.2014.11.035
  13. Singh RP, Chidambara Murthy KN, Jayaprakasha GK. Studies on the Antioxidant activity of pomegranate (Punicagranatum) peel and seed extracts using in vitro models. J Agric Food Chem 2002;50:81-6.  https://doi.org/10.1021/jf010865b
  14. Naveena BM, Sen AR, Vaithiyanathan S, Babji Y, Kondaiah N. Comparative efficacy of pomegranate juice, pomegranate rind powder extract and BHT as antioxidants in cooked chicken patties. Meat Sci 2008;80:1304-8.  https://doi.org/10.1016/j.meatsci.2008.06.005
  15. Kanatt SR, Chander R, Sharma A. Antioxidant and antimicrobial activity of pomegranate peel extract improves the shelf life of chicken products. Int J Food Sci Technol 2010;45:216-22.  https://doi.org/10.1111/j.1365-2621.2009.02124.x
  16. Jakobek L. Interactions of polyphenols with carbohydrates, lipids and proteins. Food Chem 2015;175:556-67.  https://doi.org/10.1016/j.foodchem.2014.12.013
  17. Aviram M, Dornfeld L, Rosenblat M, Volkova N, Kaplan M, Coleman R, Hayek T, Presser D, Fuhrman B. Pomegranate juice consumption reduces oxidative stress, atherogenic modifications to LDL, and platelet aggregation: studies in humans and in atherosclerotic apolipoprotein E-deficient mice. Am J Clin Nutr 2000;71:1062-76.  https://doi.org/10.1093/ajcn/71.5.1062
  18. World Health Organization. Pericarpium Granati. WHO Monographs on Selected Medicinal Plants. 42009 [Internet]. Geneva: WHO; 2006 [cited 2022 February 10]. Available from: https://apps.who.int/iris/handle/10665/42052. 
  19. Rakicioglu NT, Ayaz A, Pekcan G. Food and Food Photo Catalogue, Sizes and Quantities. Ankara: Nadir Press; 2012. 
  20. Merdol TK. Standard Food Recipes for Instituons With Mass Nutrition. Ankara: Hatipoglu Press; 2003. 
  21. Schmind M. Beslenme Bilgi Sistemi BEBIS 8.2 Paket program [Internet]. Struttgart: Entwickelt an der Universital Hohenheim; 2011 [cited 2022 February 10]. Available from: https://www.bebis.com.tr. 
  22. Pekcan G. Determination of nutritional status. In: Baysal A, Aksoy M, Besler T, editors. Diet Handbook. Ankara: Hatipoglu Press; 2013. p.67-141. 
  23. Ashwell M, Gibson S. Waist-to-height ratio as an indicator of 'early health risk': simpler and more predictive than using a 'matrix' based on BMI and waist circumference. BMJ Open 2016;6:e010159. 
  24. Grabez M, Skrbic R, Stojiljkovic MP, Vucic VM, Grujic VR, Jakovljevic V, Djuric DM, Surucic R, Savikin K, Bigovic D, et al. A prospective, randomized, double-blind, placebo-controlled trial of polyphenols on the outcomes of inflammatory factors and oxidative stress in patients with type 2 diabetes mellitus. Rev Cardiovasc Med 2022;23:57. 
  25. El-Hadary AE, Ramadan MF. Phenolic profiles, antihyperglycemic, antihyperlipidemic, and antioxidant properties of pomegranate (Punica granatum) peel extract. J Food Biochem 2019;43:e12803. 
  26. Singh B, Singh JP, Kaur A, Singh N. Phenolic compounds as beneficial phytochemicals in pomegranate (Punica granatum L.) peel: a review. Food Chem 2018;261:75-86.  https://doi.org/10.1016/j.foodchem.2018.04.039
  27. Guil-Guerrero JL, Ramos L, Moreno C, Zuniga-Paredes JC, Carlosama-Yepez M, Ruales P. Plant foods byproducts as sources of health-promoting agents for animal production: a review focusing on the tropics. Agron J 2016;108:1759-74.  https://doi.org/10.2134/agronj2015.0555
  28. Dietary Reference Intakes for Vitamin C. Vitamin E, Selenium, and Carotenoids. Washington DC: National Academies Press; 2000. p.35-58. 
  29. Yoon JH, Baek SJ. Molecular targets of dietary polyphenols with anti-inflammatory properties. Yonsei Med J 2005;46:585-96.  https://doi.org/10.3349/ymj.2005.46.5.585
  30. Amato MC, Guarnotta V, Giordano C. Body composition assessment for the definition of cardiometabolic risk. J Endocrinol Invest 2013;36:537-43. 
  31. Luo W, Guo Z, Hu X, Zhou Z, Wu M, Zhang L, Liu J. 2 years change of waist circumference and body mass index and associations with type 2 diabetes mellitus in cohort populations. Obes Res Clin Pract 2013;7:e290-6.  https://doi.org/10.1016/j.orcp.2012.02.005
  32. Azizi-Soleiman F, Khoshhali M, Heidari-Beni M, Qorbani M, Kelishadi R. Association between dietary antioxidant quality score and anthropometric measurements in children and adolescents: The weight disorders survey of the CASPIAN-IV Study. J Trop Pediatr 2021;67:fmaa065. 
  33. Vincent HK, Taylor AG. Biomarkers and potential mechanisms of obesity-induced oxidant stress in humans. Int J Obes (Lond) 2006;30:400-18.  https://doi.org/10.1038/sj.ijo.0803177
  34. Puchau B, Ochoa MC, Zulet MA, Marti A, Martinez JA, Members G. Dietary total antioxidant capacity and obesity in children and adolescents. Int J Food Sci Nutr 2010;61:713-21.  https://doi.org/10.3109/09637481003757860
  35. Hermsdorff HH, Puchau B, Volp AC, Barbosa KB, Bressan J, Zulet MA, Martinez JA. Dietary total antioxidant capacity is inversely related to central adiposity as well as to metabolic and oxidative stress markers in healthy young adults. Nutr Metab (Lond) 2011;8:59. 
  36. Yadav A, Kumari R, Yadav A, Mishra JP, Srivastava S, Prabha S. Antioxidants and its functions in human body: a review. Res Environ Life Sci 2016;9:1328-31. 
  37. Rampersaud GC, Valim MF. 100% citrus juice: nutritional contribution, dietary benefits, and association with anthropometric measures. Crit Rev Food Sci Nutr 2017;57:129-40.  https://doi.org/10.1080/10408398.2013.862611
  38. Bhargava A. Fiber intakes and anthropometric measures are predictors of circulating hormone, triglyceride, and cholesterol concentrations in the women's health trial. J Nutr 2006;136:2249-54.  https://doi.org/10.1093/jn/136.8.2249
  39. Jarvi A, Karlstrom B, Vessby B, Becker W. Increased intake of fruits and vegetables in overweight subjects: effects on body weight, body composition, metabolic risk factors and dietary intake. Br J Nutr 2016;115:1760-8.  https://doi.org/10.1017/S0007114516000970
  40. Velazquez-Lopez L, Santiago-Diaz G, Nava-Hernandez J, Munoz-Torres AV, Medina-Bravo P, Torres-Tamayo M. Mediterranean-style diet reduces metabolic syndrome components in obese children and adolescents with obesity. BMC Pediatr 2014;14:175. 
  41. Al-Muammar MN, Khan F. Obesity: the preventive role of the pomegranate (Punica granatum). Nutrition 2012;28:595-604.  https://doi.org/10.1016/j.nut.2011.11.013
  42. Hosseini B, Saedisomeolia A, Wood LG, Yaseri M, Tavasoli S. Effects of pomegranate extract supplementation on inflammation in overweight and obese individuals: A randomized controlled clinical trial. Complement Ther Clin Pract 2016;22:44-50.  https://doi.org/10.1016/j.ctcp.2015.12.003
  43. Gonzalez-Ortiz M, Martinez-Abundis E, Espinel-Bermudez MC, Perez-Rubio KG. Effect of pomegranate juice on insulin secretion and sensitivity in patients with obesity. Ann Nutr Metab 2011;58:220-3.  https://doi.org/10.1159/000330116
  44. van der Schaft N, Trajanoska K, Rivadeneira F, Ikram MA, Schoufour JD, Voortman T. Total dietary antioxidant capacity and longitudinal trajectories of body composition. Antioxidants (Basel) 2020;9:728. 
  45. Singh RP, Chidambara Murthy KN, Jayaprakasha GK. Studies on the antioxidant activity of pomegranate (Punica granatum) peel and seed extracts using in vitro models. J Agric Food Chem 2002;50:81-6.  https://doi.org/10.1021/jf010865b
  46. Asgary S, Sahebkar A, Afshani MR, Keshvari M, Haghjooyjavanmard S, Rafieian-Kopaei M. Clinical evaluation of blood pressure lowering, endothelial function improving, hypolipidemic and anti-inflammatory effects of pomegranate juice in hypertensive subjects. Phytother Res 2014;28:193-9.  https://doi.org/10.1002/ptr.4977
  47. Stockton A, Farhat G, McDougall GJ, Al-Dujaili EA. Effect of pomegranate extract on blood pressure and anthropometry in adults: a double-blind placebo-controlled randomised clinical trial. J Nutr Sci 2017;6:e39. 
  48. Aleixandre A, Miguel M. Dietary fiber and blood pressure control. Food Funct 2016;7:1864-71.  https://doi.org/10.1039/C5FO00950B
  49. Francis GA, Annicotte JS, Auwerx J. PPAR agonists in the treatment of atherosclerosis. Curr Opin Pharmacol 2003;3:186-91.  https://doi.org/10.1016/S1471-4892(03)00014-6
  50. Makino-Wakagi Y, Yoshimura Y, Uzawa Y, Zaima N, Moriyama T, Kawamura Y. Ellagic acid in pomegranate suppresses resistin secretion by a novel regulatory mechanism involving the degradation of intracellular resistin protein in adipocytes. Biochem Biophys Res Commun 2012;417:880-5.  https://doi.org/10.1016/j.bbrc.2011.12.067
  51. Chandalia M, Garg A, Lutjohann D, von Bergmann K, Grundy SM, Brinkley LJ. Beneficial effects of high dietary fiber intake in patients with type 2 diabetes mellitus. N Engl J Med 2000;342:1392-8.  https://doi.org/10.1056/NEJM200005113421903
  52. Sohrab G, Nasrollahzadeh J, Zand H, Amiri Z, Tohidi M, Kimiagar M. Effects of pomegranate juice consumption on inflammatory markers in patients with type 2 diabetes: A randomized, placebo-controlled trial. J Res Med Sci 2014;19:215-20. 
  53. Bonneau GA, Pedrozo WR, Berg G. Adiponectin and waist circumference as predictors of insulin-resistance in women. Diabetes Metab Syndr 2014;8:3-7.  https://doi.org/10.1016/j.dsx.2013.10.005
  54. Sarwar N, Gao P, Seshasai SR, Gobin R, Kaptoge S, Di Angelantonio E, Ingelsson E, Lawror DA, Selvin E, Stampfer E, et al. Diabetes mellitus, fasting blood glucose concentration, and risk of vascular disease: a collaborative meta-analysis of 102 prospective studies. Lancet 2010;375:2215-22.  https://doi.org/10.1016/S0140-6736(10)60484-9
  55. Abdel-Rahim E, El-Beltagi H, Romela R. White bean seeds and Pomegranate peel and fruit seeds as hypercholesterolemic and hypolipidemic agents in albino rats. Grasas Aceites 2013;64:50-8.  https://doi.org/10.3989/gya.095412
  56. Rosenblat M, Aviram M. Pomegranate juice protects macrophages from triglyceride accumulation: inhibitory effect on DGAT1 activity and on triglyceride biosynthesis. Ann Nutr Metab 2011;58:1-9.  https://doi.org/10.1159/000323096
  57. Lv O, Wang L, Li J, Ma Q, Zhao W. Effects of pomegranate peel polyphenols on lipid accumulation and cholesterol metabolic transformation in L-02 human hepatic cells via the PPARγ-ABCA1/CYP7A1 pathway. Food Funct 2016;7:4976-83.  https://doi.org/10.1039/C6FO01261B
  58. Hontecillas R, Diguardo M, Duran E, Orpi M, Bassaganya-Riera J. Catalpic acid decreases abdominal fat deposition, improves glucose homeostasis and upregulates PPAR α expression in adipose tissue. Clin Nutr 2008;27:764-72.  https://doi.org/10.1016/j.clnu.2008.07.007
  59. Jang A, Srinivasan P, Lee NY, Song HP, Lee JW, Lee M, Jo C. Comparison of hypolipidemic activity of synthetic gallic acid-linoleic acid ester with mixture of gallic acid and linoleic acid, gallic acid, and linoleic acid on high-fat diet induced obesity in C57BL/6 Cr Slc mice. Chem Biol Interact 2008;174:109-17.  https://doi.org/10.1016/j.cbi.2008.05.018
  60. Sahebkar A, Simental-Mendia LE, Giorgini P, Ferri C, Grassi D. Lipid profile changes after pomegranate consumption: a systematic review and meta-analysis of randomized controlled trials. Phytomedicine 2016;23:1103-12.  https://doi.org/10.1016/j.phymed.2015.12.014
  61. Grassi D, Desideri G, Ferri L, Tiberti S, Ferri C. Cocoa and lipid profile: a fat paradox? Agro Food Ind Hi Tech 2009;20:23-5. 
  62. Guo C, Wei J, Yang J, Xu J, Pang W, Jiang Y. Pomegranate juice is potentially better than apple juice in improving antioxidant function in elderly subjects. Nutr Res 2008;28:72-7.  https://doi.org/10.1016/j.nutres.2007.12.001
  63. Petrovic S, Arsic A, Glibetic M, Cikiriz N, Jakovljevic V, Vucic V. The effects of polyphenol-rich chokeberry juice on fatty acid profiles and lipid peroxidation of active handball players: results from a randomized, double-blind, placebo-controlled study. Can J Physiol Pharmacol 2016;94:1058-63.  https://doi.org/10.1139/cjpp-2015-0575
  64. Kojadinovic MI, Arsic AC, Debeljak-Martacic JD, Konic-Ristic AI, Kardum ND, Popovic TB, Glibetic MD. Consumption of pomegranate juice decreases blood lipid peroxidation and levels of arachidonic acid in women with metabolic syndrome. J Sci Food Agric 2017;97:1798-804.  https://doi.org/10.1002/jsfa.7977
  65. Ardekani MR, Hajimahmoodi M, Oveisi MR, Sadeghi N, Jannat B, Ranjbar AM, Gholam N, Moridi T. Comparative antioxidant activity and total flavonoid content of Persian pomegranate (Punica granatum L.) cultivars. Iran J Pharm Res 2011;10:519-24. 
  66. Tehranifar A, Selahvarzi Y, Kharrazi M, Bakhsh VJ. High potential of agro-industrial by-products of pomegranate (Punica granatum L.) as the powerful antifungal and antioxidant substances. Ind Crops Prod 2011;34:1523-7.  https://doi.org/10.1016/j.indcrop.2011.05.007
  67. Lopez-Marcos MC, Bailina C, Viuda-Martos M, Perez-Alvarez JA, Fernandez-Lopez J. Properties of dietary fibers from agroindustrial coproducts as source for fiber-enriched foods. Food Bioprocess Technol 2015;8:2400-8.  https://doi.org/10.1007/s11947-015-1591-z
  68. Xu X, Zhang J, Zhang Y, Qi H, Wang P. Associations between dietary fiber intake and mortality from all causes, cardiovascular disease and cancer: a prospective study. J Transl Med 2022;20:344. 
  69. Baslar M, Ertugay MF. Effect of ultrasound and photosonication treatment on polyphenoloxidase (PPO) activity, total phennolic component and colour of apple juice. Int J Food Sci Technol 2013;48:886-92.  https://doi.org/10.1111/ijfs.12015
  70. Topcu B, Caba ZT, Erdil DN. Effect of oat bread production stages on phenolic content and antioxidant activity. Food Health 2019;5:48-63.  https://doi.org/10.3153/FH19006
  71. Sablani SS, Marcotte M, Baik OD, Castaigne F. Modeling of Simultaneous heat and water transport in the baking process. Lebensm Wiss Technol 1998;31:201-9.  https://doi.org/10.1006/fstl.1997.0360
  72. Eliasova M, Kotikova Z, Lachman J, Orsak M, Martinek P. Influence of baking on anthocyanin content in coloured-grain wheat bread. Plant Soil Environ 2020;66:381-6.  https://doi.org/10.17221/210/2020-PSE
  73. Han HM, Koh BK. Antioxidant activity of hard wheat flour, dough and bread prepared using various processes with the addition of different phenolic acids. J Sci Food Agric 2011;91:604-8.  https://doi.org/10.1002/jsfa.4188
  74. Hobbs RJ, Higgs E, Hall CM, Bridgewater P, Chapin FS, Ellis EC, Ewel JJ, Hallett M, Harris J, Hulvey KB, et al. Managing the whole landscape: historical, hybrid, and novel ecosystems. Front Ecol Environ 2014;12:557-64.  https://doi.org/10.1890/130300
  75. Altunkaya A, Hedegaard RV, Brimer L, Gokmen V, Skibsted H. Antioxidant capacity versus chemical safety of wheat bread enriched with pomegranate peel powder. Food Funct 2013;4:722-7.  https://doi.org/10.1039/c3fo30296b
  76. Srivastava P, Indrani D, Singh RP. Effect of dried pomegranate (Punica granatum) peel powder (DPPP) on textural, organoleptic and nutritional characteristics of biscuits. Int J Food Sci Nutr 2014;65:827-33.  https://doi.org/10.3109/09637486.2014.937797