The ability of yoghurt supplemented with dietary fibers or brans extracted from wheat or rice to reduce serum lipids and enhance liver function in male hypercholesterolemic rats
Corresponding Author
Nassra Dabour
Functional Foods and Nutraceuticals Laboratory (FFNL), Department of Dairy Science and Technology, Faculty of Agriculture, University of Alexandria, Alexandria, Egypt
Correspondence
Nassra Dabour, Functional Foods and Nutraceuticals Laboratory (FFNL), Department of Dairy Science and Technology, Faculty of Agriculture, University of Alexandria, 21545 Alexandria, Egypt.
Email: [email protected]
Search for more papers by this authorKhaled Elsaadany
Functional Foods and Nutraceuticals Laboratory (FFNL), Department of Dairy Science and Technology, Faculty of Agriculture, University of Alexandria, Alexandria, Egypt
Search for more papers by this authorEnaam Shoukry
Functional Foods and Nutraceuticals Laboratory (FFNL), Department of Dairy Science and Technology, Faculty of Agriculture, University of Alexandria, Alexandria, Egypt
Search for more papers by this authorSaeed Hamdy
Functional Foods and Nutraceuticals Laboratory (FFNL), Department of Dairy Science and Technology, Faculty of Agriculture, University of Alexandria, Alexandria, Egypt
Search for more papers by this authorAmel Taïbi
Nutritional Sciences, Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada
Search for more papers by this authorEhab Kheadr
Functional Foods and Nutraceuticals Laboratory (FFNL), Department of Dairy Science and Technology, Faculty of Agriculture, University of Alexandria, Alexandria, Egypt
Search for more papers by this authorCorresponding Author
Nassra Dabour
Functional Foods and Nutraceuticals Laboratory (FFNL), Department of Dairy Science and Technology, Faculty of Agriculture, University of Alexandria, Alexandria, Egypt
Correspondence
Nassra Dabour, Functional Foods and Nutraceuticals Laboratory (FFNL), Department of Dairy Science and Technology, Faculty of Agriculture, University of Alexandria, 21545 Alexandria, Egypt.
Email: [email protected]
Search for more papers by this authorKhaled Elsaadany
Functional Foods and Nutraceuticals Laboratory (FFNL), Department of Dairy Science and Technology, Faculty of Agriculture, University of Alexandria, Alexandria, Egypt
Search for more papers by this authorEnaam Shoukry
Functional Foods and Nutraceuticals Laboratory (FFNL), Department of Dairy Science and Technology, Faculty of Agriculture, University of Alexandria, Alexandria, Egypt
Search for more papers by this authorSaeed Hamdy
Functional Foods and Nutraceuticals Laboratory (FFNL), Department of Dairy Science and Technology, Faculty of Agriculture, University of Alexandria, Alexandria, Egypt
Search for more papers by this authorAmel Taïbi
Nutritional Sciences, Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada
Search for more papers by this authorEhab Kheadr
Functional Foods and Nutraceuticals Laboratory (FFNL), Department of Dairy Science and Technology, Faculty of Agriculture, University of Alexandria, Alexandria, Egypt
Search for more papers by this authorAbstract
This study was undertaken to evaluate the effect of yoghurt supplementation with rice and wheat brans or dietary fibers on serum lipid profile, liver, and heart functionalities, and hepatopathological aspects of the liver of hypercholesterolemic rats. 48 male rats were divided into 8 groups. Group 1 was kept as negative control and fed with a standard diet, and groups 2 to 6 were fed a hypercholesterolemia-induced diet supplemented with brans or dietary fibers of both grains. G2 received yoghurt without supplementation. The experiment lasted for 4 weeks. Results revealed that hypercholesterolemic rats administrated yoghurt supplemented with brans or dietary fibers reduced serum glucose from 113.9 ± 2.72 to 85.5 ± 4.94 in the serum of animals that received dietary fibers of rice and wheat, respectively. In addition, lipids profile and liver antioxidant status were improved. In addition, liver and heart functionalities and liver histopathological architecture were all improved depending on the type of administrated brans or fibers added to yoghurt. The inclusion of 0.5% of rice or wheat brans could be recommended to be added to yoghurt.
Practical applications
Yoghurt is the most famous fermented milk in the world. Supplementation of yoghurt with rice and wheat brans or dietary fibers increased its nutritional value. We proved that this new product contributes to reducing serum glucose, improving lipids profile, and enhancing liver and heart functions in hypercholesterolemic rats. This study confirmed the suitability to add a thesis type of brans or dietary fibers as bioactive ingredients to yoghurt and increased the varieties of functional foods.
CONFLICT OF INTEREST
The authors declare that they have no known competing financial interests or personal relationships that could influence the work presented in this paper.
Open Research
DATA AVAILABILITY STATEMENT
Not applicable.
REFERENCES
- Abulnaja, K. O., & El-Rabey, H. A. (2015). The efficiency of barley (Hordeum vulgare) bran in ameliorating blood and treating fatty heart and liver of male rats. Evidence-based Complementary and Alternative Medicine, 2015, 740716. https://doi.org/10.1155/2015/740716
- Aebi, H. (1984). Catalase in vitro. Methods in Enzymology, 105, 121–126. https://doi.org/10.1016/s0076-6879(84)05016-3
- Allain, C. C., Poon, L. S., Chan, C. S. G., Richmond, W., & Fu, P. C. (1974). Enzymatic determination of total serum cholesterol. Clinical Chemistry Journal, 20, 470–475. https://doi.org/10.1093/clinchem/20.4.470
- AOAC. (1990). Official methods of analysis ( 15th ed.). Association of Official Analysis Chemists Inc.
- Assmann, G., & Nofer, J. (2003). Atheroprotective effects of high-density lipoproteins. Annual Review of Medicine, 54, 321–341. https://doi.org/10.1146/annurev.med.54.101601.152409
- Bancroft, J. D., & Gamble, M. (2002). Theory and practice of histological techniques. In B. Swisher (Ed.), Microorganisms (pp. 325–344). Churchill.
- Bazzano, L. A., Thompson, A. M., Tees, M. T., Nguyen, C. H., & Winham, D. M. (2011). Non-soy legume consumption lowers cholesterol levels: A meta analysis of randomized controlled trials. Nutrition, Metabolism and Cardiovascular Diseases, 21, 94–103. https://doi.org/10.1038/oby.2005.240
- Bergmeyer, H. U. (1985). Methods of enzymatic analysis, methods of enzymatic analysis: Volume 8: Metabolites 3: Lipids, amino acids and related compounds (Vol. 8). Wiley-Blackwell.
- Braham, D., & Trinder, P. (1972). Methods for determination of blood glucose level by spectrophotometer. Analyst, 97, 142–145. https://doi.org/10.1039/an9729700142
- Childs, A. C., Phaneuf, S. L., Dirks, A. J., Philips, T., & Leeuwenburgh, C. (2002). Doxorubicin treatment in vivo causes cytochrome C release and cardiomyocyte apoptosis, as well as increased mitochondrial efficiency, superoxide dismutase activity, and Bcl-2: Bax ratio. Cancer Research, 62, 4592–4598.
- Choi, S. Y., Park, J. S., & Jung, W. T. (2011). A study on the shrinkage control of fiber reinforced concrete pavement. Procedia Engineering, 14, 2815–2822. https://doi.org/10.1016/j.proeng.2011.07.354
- Claye, S. S., Idouraine, A., & Weber, C. W. (1996). In vitro mineral binding capacity of five fiber sources and their insoluble components for copper and zinc. Plant Foods for Human Nutrition, 49, 257–269. https://doi.org/10.1007/BF01091975
- Dabija, A., Codină, G. G., Gâtlan, A.-M., & Rusu, L. (2018). Quality assessment of yogurt enriched with different types of fibers. CyTA—Journal of Food, 16, 859–867. https://doi.org/10.1080/19476337.2018.1483970
- Dabour, N., Dyab, N., & Kheadr, E. (2019). Iron fortification of reduced-fat bioyoghurt containing either short- or long-chain inulin. International Journal of Dairy Technology, 72, 229–239. https://doi.org/10.1111/1471-0307.12575
- Demirci, T., Aktaş, K., Sözeri, D., Öztürk, H. I., & Akına, N. (2017). Rice bran improve probiotic viability in yoghurt and provide added antioxidative benefits. Journal of Functional Foods, 36, 396–403. https://doi.org/10.1016/J.JFF.2017.07.019
- Dobiásová, M. (2006). AIP-atherogenic index of plasma as a significant predictor of cardiovascular risk: From research to practice. Vnitr Lek, 52, 64–71 (in Czech).
- El-Rabey, A. H., Al-Seeni, N. M., & Al-Ghamdi, B. H. (2017). Comparison between the hypolipidemic activity of parsley and carob in hypercholesterolemic male rats. BioMed Research International, 2017, 3098745. https://doi.org/10.1155/2013/263594
- El-Rabey, H. A., Al-Seeni, M. N., & Amer, H. M. (2013). Efficiency of barley bran and oat bran in ameliorating blood lipid profile and the adverse histological changes in hypercholesterolemic male rats. BioMed Research International, 2013, 263495. https://doi.org/10.1155/2013/263594
- Elsaadany, K., & Abd-Elhaleem, H.-A. (2019). In vivo anti-hypercholesterolemic effect of buttermilk, milk fat globule membrane and Enterococcus faecium FFNL-12. Current Research in Nutrition and Food Science, 7, 517–531. https://doi.org/10.12944/CRNFSJ.7.2.21
- Encarnação, J. C., Abrantes, A. M., Pires, A. S., & Botelho, M. F. (2015). Revisit dietary fiber on colorectal cancer: Butyrate and its role on prevention and treatment. Cancer Metastasis Review, 34, 465–478. https://doi.org/10.1007/s10555-015-9578-9
- Eng, H. Y., & Rozalli, N. H. M. (2022). Rice bran and its constituents: Introduction and potential food uses. International Journal of Food Science and Technology, 57, 4041–4051. https://doi.org/10.1111/ijfs.15808
- Fardet, A. (2010). New hypotheses for the health-protective mechanisms of whole-grain cereals: What is beyond fibre? Nutrition Research Reviews, 23, 65–134. https://doi.org/10.1017/S0954422410000041
- Food and Agriculture Organization (FAO). (2021). http://www.fao.org/worldfoodsituation/csdb/en/
- Fossati, P., & Prencipe, L. (1982). Serum triglycerides determined calorimetrically with an enzyme that produces hydrogen peroxide. Journal of Clinical Chemistry, 28, 2077–2080.
- Friedewald, W. T., Levy, R. I., & Fredrickson, D. S. (1972). Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clinical Chemistry, 18, 499–502.
- Gowd, V., Xie, L., Zheng, X., & Chen, W. (2019). Dietary fibers as emerging nutritional factors against diabetes: Focus on the involvement of gut microbiota. Critical Reviews in Biotechnology, 39, 524–540. https://doi.org/10.1080/07388551.2019.1576025
- Grove, T. H. (1979). The effect of reagent pH on determination of high-density lipoprotein cholesterol by precipitation of with sodium phosphotungstate-magnesium. Journal of Clinical Chemistry, 25, 560–564.
- Gürgün, C., Ildızlı, M., Yavuzgil, O., Sin, A., Apaydin, A., Cinar, C., & Kultursay, H. (2008). The effects of short term statin treatment on left ventricular function and inflammatory markers in patients with chronic heart failure. The International Journal of Cardiology, 123, 102–107. https://doi.org/10.1016/j.ijcard.2006.11.152
- Harnafi, H., Caid, H. S., Bouanani, N. H., Aziz, M., & Amrani, S. (2008). Hypolipemic activity of polyphenol-rich extracts from Ocimum basilicum in triton WR-1339-induced hyperlipidemic mice. Food Chemistry, 108, 205–212. https://doi.org/10.1016/j.foodchem.2007.10.062
- Hassan, S., Abd El-Twab, S., Hetta, M., & Mahmoud, B. (2011). Improvement of lipid profile and antioxidant of hypercholesterolemic albino rats by polysaccharides extracted from the green alga Ulva lactuca Linnaeus. Saudi Journal of Biological Sciences, 18, 333–340. https://doi.org/10.1016/j.sjbs.2011.01.005
- Herman-Lara, E., Elvira-Torales, L. I., Rodriguez-Miranda, J., Torruco-Uco, J. G., Car- mona-García, R., Mendoza-García, P. G., García, H. S., & Soto-Rodríguez, I. (2014). Impact of micronized starfruit (Averrhoa carambola) fiber concentrate on lipid metabolism in mice. International Journal of Food Science Nutrition, 65, 862–867. https://doi.org/10.3109/09637486.2014.918590
- Hewawasam, R. P., Jayatilaka, K. A., Pathirana, C., & Mudduwa, L. K. (2004). Hepatoprotective effect of Epaltes divaricata extract on carbon tetrachloride induced hepatotoxicity in mice. The Indian Journal of Medical Research, 120, 30–34.
- Hodis, N. H. (1999). Triglyceride-rich lipoprotein remnant particles and risk of atherosclerosis. Circulation, 99, 2852–2854.
- Hundemer, J. K., Nabar, S. P., Shriver, B. J., & Forman, L. P. (1991). Dietary fiber sources lower blood cholesterol in C57BL/6 mice. Journal of Nutrition, 121, 1360–1365. https://doi.org/10.1093/jn/121.9.1360
- Hussien, A. M., Abbas, M. H., Bayoumi, M. H., & Abd El-Aziz, M. (2017). Properties of full fat rice bran and yoghurt fortified with it. International Journal of Dairy Science, 12, 170–176. https://doi.org/10.3923/ijds.2017.170.176
- IFCC. (1989). Methods for the measurement of catalytic concentration of enzymes. part 7: IFCC method for creatine kinase. Japan Information and Culture Centre, 9, 130–139.
- Islam, M. S., Islam, M. K., Das, S. K., & Hossain, M. M. (2014). Effects of butter on blood biotchemistry and histotexure of heart in the development of obesity in Swiss albino mice. Bangladesh Journal for Veterinary Medicin, 12, 203–209. https://doi.org/10.3329/bjvm.v12i2.21293
10.3329/bjvm.v12i2.21293 Google Scholar
- Kim, G. W., Ahn, K. Y., Kim, Y. H., & Jeong, G. W. (2016). Time-course metabolic changes in high-fat diet-induced obesity rats: A pilot study using hyperpolarized (13) C dynamic MRS. Magnetic Resonance Imaging, 34, 1199–1205. https://doi.org/10.1016/j.mri.2016.06.002
- Lakmal, K., Yasawardene, P., Jayarajah, U., & Seneviratne, S. L. (2021). Nutritional and medicinal properties of Star fruit (Averrhoa carambola): A review. Food Science and Nutrition, 9, 1810–1823. https://doi.org/10.1002/fsn3.2135
- Lattimer, J. M., & Haub, M. D. (2010). Effects of dietary fiber and its components on metabolic health. Nutrients, 2, 1266–1289. https://doi.org/10.3390/nu2121266
- Liu, M., Zhang, M., Ye, H., Lin, S., Yang, Y., Wang, L., Jones, G., & Trang, H. (2013). Multiple toxicity studies of trehalose in mice by intragastric administration. Food Chemistry, 136, 485–490. https://doi.org/10.1016/j.foodchem.2012.09.031
- Macher, S., Drexler, C., Lindenau, I., Sareban, N., Schlenke, P., & Amrein, K. (2016). High-dose intravenously administered iron versus orally administered iron in blood donors with iron deficiency: Study protocol for a randomised controlled trial. Trials, 17, 527–533. https://doi.org/10.1186/s13063-016-1648-y
- Misra, H. P., & Fridovich, I. (1972). The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. Journal of Biological Chemistry, 247, 3170–3175.
- Mohammed, O., Dyab, N., Kheadr, E., & Dabour, N. (2021). Effectiveness of inulin-type on the iron bioavailability in anemic female rats fed bio-yogurt. RSC Advances, 11, 1928–1938. https://doi.org/10.1039/d0ra08873k
- Moss, D. W., Henderson, A. R., & Kachmar, J. F. (1987). Enzymes. In N. W. Tietz (Ed.), Fundamentals of clinical chemistry ( 3rd ed., pp. 346–421). Saunders.
- Müller, M., Canfora, E. E., & Blaak, E. E. (2018). Gastrointestinal transit time, glucose homeostasis and metabolic health: Modulation by dietary fibers. Nutrients, 10, 275. https://doi.org/10.3390/nu10030275
- National Research Council. (2011). Guide for the care and use of laboratory animals ( 8th ed.). The National Academies Press.
- Niu, Y., Xie, Z., Zhang, H., Sheng, Y., & Yu, L. (2013). Effects of structural modifications on physicochemical and bile acid-binding properties of psyllium. Journal of Agricultural and Food Chemistry, 61, 596–601. https://doi.org/10.1021/jf3043117
- Ohkawa, H., Ohishi, N., & Yagi, K. (1979). Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Analytical Biochemistry, 95, 351–358. https://doi.org/10.1016/0003-2697(79)90738-3
- Sharif, M. K., Butt, M. S., Anjum, F. M., & Khan, S. H. (2014). Rice bran: A novel functional ingredient. Critical Reviews in Food Science and Nutrition, 54, 807–816. https://doi.org/10.1080/10408398.2011.608586
- Shewry, P. (2009). The Healthgrain programme opens new opportunities for improving wheat for nutrition and health. Nutrtion Bulletin, 34, 225–231. https://doi.org/10.1111/j.1467-3010.2009.01747.x
10.1111/j.1467?3010.2009.01747.x Google Scholar
- Soliman, G. A. (2019). Dietary fiber, atherosclerosis, and cardiovascular disease. Nutrients, 11, 1155. https://doi.org/10.3390/nu11051155
- Song, H. Y., Mao, Z. M., Yang, L. L., Liu, T., Li, D. F., Zhang, L., Ge, Y. L., Zheng, P. Y., Liu, P., Zhang, X. Q., & Ji, G. (2011). Dangfei liganning capsules attenuate the susceptibility of rat nonalcoholic fatty liver to carbon tetrachloride toxicity. Journal of Traditional Chinese Medicine, 31, 327–333. https://doi.org/10.1016/s0254-6272(12)60013-2
- Tangeda, P. R., Patil, S., Shastr, N., & Noorali, S. N. (2016). Maternal myocardial performance in second trimester of pregnancy with iron deficiency anemia. Journal of Clinical and Diagnostic Research, 10, CC16–CC18. https://doi.org/10.7860/JCDR/2016/17774.7507
- Tietz, N. W., Rinker, A. D., & Shaw, L. M. (1983). IFCC methods for the measurement of catalytic concentration of enzymes Part 5. IFCC method for alkaline phosphatase (orthophosphoricmonoester phosphohydrolase, alkaline optimum, EC 3.1.3.1). Journal of Clinical Chemistry and Clinical Biochemistry, 21, 731–748.
- Trowell, H. (1972). Ischemic heart disease and dietary fiber. The American Journal of Clinical Nutrition, 25, 926–932. https://doi.org/10.1093/ajcn/25.9.926
- Van Soest, P. V., Robertson, J., & Lewis, B. (1991). Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. Journal of Dairy Science, 74, 3583–3597. https://doi.org/10.3168/jds.S0022-0302(91)78551-2
- Verd, J. C., Peris, C., Alegret, M., Díaz, C., Hernández, G., Vázquez, M., Adzet, T., Laguna, J. C., & Sánchez, R. M. (1999). Different effect of simvastatin and atorvastatin on key enzymes involved in VLDL synthesis and catabolism in high fat/cholesterol fed rabbits. British Journal of Pharmacology, 127, 1479–1485. https://doi.org/10.1038/sj.bjp.0702668
- Wang, J., Shimada, M., Kato, Y., Kusada, M., & Nagaoka, S. (2015). Cholesterol-lowering effect of rice bran protein containing bile acid-binding proteins. Bioscience, Biotechnology, and Biochemistry, 79, 456–461. https://doi.org/10.1080/09168451.2014.978260
- Weickert, M. O., & Pfeiffer, A. F. (2008). Metabolic effects of dietary fiber consumption and prevention of diabetes. The Journal of Nutrition, 138, 439–442. https://doi.org/10.1093/jn/138.3.439
- Wikan, N., Tocharus, J., Sivasinprasasn, S., Kongkaew, A., Chaichompoo, W., Suksamrarn, A., & Tocharus, C. (2020). Capsaicinoid nonivamide improves nonalcoholic fatty liver disease in rats fed a high-fat diet. Journal of Pharmacological Sciences, 143, 188–198. https://doi.org/10.1016/j.jphs.2020.03.008
- World Health Organization. (2021). Cardiovascular diseases (CVDs). https://www.who.int/newsrom/fact-sheets/detail/cardiovascular-diseases-(cvds)
- Wu, W., Xiao, Z., An, W., Dong, Y., & Zhang, B. (2018, May 24). Dietary sodium butyrate improves intestinal development and function by modulating the microbial community in broilers. PLoS One. https://doi.org/10.1371/journal.pone.0197762
- Zhao, Y., Jayachandran, M., & Xu, B. (2020). In vivo antioxidant and anti-inflammatory effects of soluble dietary fiber Konjac glucomannan in type-2 diabetic rats. International Journal of Biological Macromolecules, 159, 1186–1196. https://doi.org/10.1016/j.ijbiomac.2020.05.105
- Zhi, N.-N., Zong, K., Thakur, K., Qu, J., Shi, J.-J., Yang, J.-L., Yao, J., & Wei, Z.-J. (2018). Development of a dynamic prediction model for shelf-life evaluation of yogurt by using physicochemical, microbiological and sensory parameters. CyTA—Journal of Food, 16, 42–49. https://doi.org/10.1080/19476337.2017.1336572
- Zollner, N., & Krish, K. (1962). Ueber die quantitative bestimnung von lipoiden (mikromethod) mittels der vielen naturlichel lipoiden (allen bekannten plasmalipoiden) gemeisamen sulphophosphovanillin-reaktion. Zeitschrift fur die Gesamte Experimentelle Medizin, 135, 545–561. https://doi.org/10.1007/BF02045455