Journal of Food and Nutrition Research
ISSN (Print): 2333-1119 ISSN (Online): 2333-1240 Website: http://www.sciepub.com/journal/jfnr Editor-in-chief: Prabhat Kumar Mandal
Open Access
Journal Browser
Go
Journal of Food and Nutrition Research. 2021, 9(7), 329-341
DOI: 10.12691/jfnr-9-7-2
Open AccessArticle

Beneficial Effects of Macaroni Made with Resistant Starch Type 4 from Unripe Banana and Turmeric Extract on Blood Clinical Chemistry and Gut Microbiota of Healthy Rats

Wongsakan Chuathong1, Wathinee Phomsakha Na Sakonnakhon2, Atitayaporn Lilakhon1, Natthaporn Devahastin Na Ayudhaya1, Worapong Khaodee1, Singkome Tima3, 4, Nutjeera Intasai3, 4, Rujirek Chaiwongsa4, 5, Sawitree Chiampanichayakul3, 4, Khanittha Punturee1, 4 and Ratchada Cressey1, 4,

1Division of Clinical Chemistry, Department of Medical Technology, Faculty of Associated Medical Sciences, Chiang Mai University, Thailand

2Laboratory Animal Center, Chiang Mai University, Thailand

3Division of Clinical Microscopy, Department of Medical Technology, Faculty of Associated Medical Sciences, Chiang Mai University, Thailand

4Cancer Research Unit of Associated Medical Sciences (AMS-CRU), Faculty of Associated Medical Sciences, Chiang Mai University, Chiang Mai 50200, Thailand

5Division of Blood Transfusion Science, Department of Medical Technology, Faculty of Associated Medical Sciences, Chiang Mai University, Thailand

Pub. Date: July 04, 2021

Cite this paper:
Wongsakan Chuathong, Wathinee Phomsakha Na Sakonnakhon, Atitayaporn Lilakhon, Natthaporn Devahastin Na Ayudhaya, Worapong Khaodee, Singkome Tima, Nutjeera Intasai, Rujirek Chaiwongsa, Sawitree Chiampanichayakul, Khanittha Punturee and Ratchada Cressey. Beneficial Effects of Macaroni Made with Resistant Starch Type 4 from Unripe Banana and Turmeric Extract on Blood Clinical Chemistry and Gut Microbiota of Healthy Rats. Journal of Food and Nutrition Research. 2021; 9(7):329-341. doi: 10.12691/jfnr-9-7-2

Abstract

Unripe banana is rich with resistant starch (RS) and this non-processed food confers many health benefits. However, unripe banana is not consumed directly and when cooked its native RS is rendered digestible. We have developed macaroni from chemically modified unripe banana flour (RS4), which maintains their content of resistant starch after being cooked, with and without the supplementation of turmeric extract. We hypothesized that consuming our banana RS4 macaroni would confer beneficial effects on metabolic profiles. Healthy Wistar rats were fed for 6 weeks with cooked banana RS4 macaroni, with and without the turmeric extract supplementation, and compared to rats fed with standard wheat macaroni. No significant physiological differences between groups were observed except rats that consumed banana RS4 macaroni had significantly smaller stomachs (p<0.05). Rats receiving banana RS4 macaroni had significantly lower triglyceride levels (p<0.05) and a trend for lower fasting blood glucose and increased expression of insulin-like growth factor-2 in theirs livers. Although it was not statistically significant, turmeric supplementation showed a trend of reducing serum total cholesterol and LDL-cholesterol as well as liver expression levels of genes involved in cholesterol metabolism, HMG CoA reductase (HMGR) and LDL-receptor related protein-1 (LRP-1). Banana RS4 macaroni did not significantly change fecal microbiota, nevertheless, addition of turmeric extract significantly increased alpha diversity and the relative abundance of Lachnospiraceae Erysipelotrichaceae and Clostridiaceae. In conclusion, the consumption of banana RS4 macaroni by healthy rats receiving a regular diet improved their blood chemistry profile associated with metabolic syndrome, and the addition of turmeric extract can significantly alter fecal microbiota.

Keywords:
metabolic syndrome functional foods Resistant Starch type 4 (RS4) unripe banana flour gut microbiota turmeric

Creative CommonsThis work is licensed under a Creative Commons Attribution 4.0 International License. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

Figures

Figure of 8

References:

[1]  The metabolic syndrome: mechanisms, epidemiology, and clinical implications. Postgrad Med. 2003; 114 (6 Suppl Managing Metabolic): 17-27.
 
[2]  Lyte M, Chapel A, Lyte JM, Ai Y, Proctor A, Jane JL, et al. Resistant Starch Alters the Microbiota-Gut Brain Axis: Implications for Dietary Modulation of Behavior. PLoS One. 2016; 11(1): e0146406.
 
[3]  Yang X, Darko KO, Huang Y, He C, Yang H, He S, et al. Resistant Starch Regulates Gut Microbiota: Structure, Biochemistry and Cell Signalling. Cell Physiol Biochem. 2017; 42(1): 306-18.
 
[4]  Liu H, Zhang M, Ma Q, Tian B, Nie C, Chen Z, et al. Health beneficial effects of resistant starch on diabetes and obesity via regulation of gut microbiota: a review. Food Funct. 2020; 11(7): 5749-67.
 
[5]  Peres J. Resistant starch may reduce colon cancer risk from red meat. J Natl Cancer Inst. 2014; 106(10).
 
[6]  Le Leu RK, Brown IL, Hu Y, Esterman A, Young GP. Suppression of azoxymethane-induced colon cancer development in rats by dietary resistant starch. Cancer Biol Ther. 2007; 6(10): 1621-6.
 
[7]  Koh GY, Rowling MJ, Schalinske KL, Grapentine K, Loo YT. Consumption of Dietary Resistant Starch Partially Corrected the Growth Pattern Despite Hyperglycemia and Compromised Kidney Function in Streptozotocin-Induced Diabetic Rats. Journal of agricultural and food chemistry. 2016; 64(40): 7540-5.
 
[8]  Zhou Z, Wang F, Ren X, Wang Y, Blanchard C. Resistant starch manipulated hyperglycemia/hyperlipidemia and related genes expression in diabetic rats. Int J Biol Macromol. 2015; 75: 316-21.
 
[9]  Trachsel J, Briggs C, Gabler NK, Allen HK, Loving CL. Dietary Resistant Potato Starch Alters Intestinal Microbial Communities and Their Metabolites, and Markers of Immune Regulation and Barrier Function in Swine. Front Immunol. 2019; 10: 1381.
 
[10]  Barouei J, Bendiks Z, Martinic A, Mishchuk D, Heeney D, Hsieh YH, et al. Microbiota, metabolome, and immune alterations in obese mice fed a high-fat diet containing type 2 resistant starch. Mol Nutr Food Res. 2017; 61(11).
 
[11]  Birt DF, Boylston T, Hendrich S, Jane JL, Hollis J, Li L, et al. Resistant starch: promise for improving human health. Adv Nutr. 2013; 4(6): 587-601.
 
[12]  Upadhyaya B, McCormack L, Fardin-Kia AR, Juenemann R, Nichenametla S, Clapper J, et al. Impact of dietary resistant starch type 4 on human gut microbiota and immunometabolic functions. Sci Rep. 2016; 6: 28797.
 
[13]  Maningat CC, Seib PA. RS4-Type Resistant Starch: Chemistry, Functionality and Health Benefits. In: Shi YC, Maningat CC, editors. In Resistant Starch: Sources, Applications and Health Benefits. NJ, USA: John Wiley & Sons; 2013. p. 43-77.
 
[14]  Rodríguez-Ambriza SL, Islas-Hernándeza JJ, Agama-Acevedo E, Tovarb J, Bello-Pérez LA. Characterization of a fibre-rich powder prepared by liquefaction of unripe banana flour. Food Chem. 2008; 107(4): 15151-21.
 
[15]  Adedayo BC, Oboh G, Oyeleye SI, Olasehinde TA. Antioxidant and Antihyperglycemic Properties of Three Banana Cultivars (Musa spp.). Scientifica (Cairo). 2016; 2016: 8391398.
 
[16]  Anyasi TA, Jideani AIO, McHau GRA. Phenolics and essential mineral profile of organic acid pretreated unripe banana flour. Food Res Int. 2018; 104: 100-9.
 
[17]  Wang J, Huang JH, Cheng YF, Yang GM. Banana resistant starch and its effects on constipation model mice. J Med Food. 2014; 17(8): 902-7.
 
[18]  Langkilde AM, Champ M, Andersson H. Effects of high-resistant-starch banana flour (RS(2)) on in vitro fermentation and the small-bowel excretion of energy, nutrients, and sterols: an ileostomy study. The American journal of clinical nutrition. 2002; 75(1): 104-11.
 
[19]  Rosado CP, Rosa VHC, Martins BC, Soares AC, Santos IB, Monteiro EB, et al. Resistant starch from green banana (Musa sp.) attenuates non-alcoholic fat liver accumulation and increases short-chain fatty acids production in high-fat diet-induced obesity in mice. Int J Biol Macromol. 2020; 145: 1066-72.
 
[20]  Shinde T, Perera AP, Vemuri R, Gondalia SV, Beale DJ, Karpe AV, et al. Synbiotic supplementation with prebiotic green banana resistant starch and probiotic Bacillus coagulans spores ameliorates gut inflammation in mouse model of inflammatory bowel diseases. Eur J Nutr. 2020.
 
[21]  Singh B, Singh JP, Kaur A, Singh N. Bioactive compounds in banana and their associated health benefits - A review. Food Chem. 2016; 206: 1-11.
 
[22]  Zhang PY, Whistler RL, BeMiller JN, Hamaker BR. Banana starch: production, physicochernical properties, and digestibility - a review. Carbohyd Polym. 2005; 59(4): 443-58.
 
[23]  Nelson KM, Dahlin JL, Bisson J, Graham J, Pauli GF, Walters MA. The Essential Medicinal Chemistry of Curcumin. J Med Chem. 2017; 60(5): 1620-37.
 
[24]  Azhdari M, Karandish M, Mansoori A. Metabolic benefits of curcumin supplementation in patients with metabolic syndrome: A systematic review and meta-analysis of randomized controlled trials. Phytother Res. 2019; 33(5): 1289-301.
 
[25]  Si X, Zhou Z, Strappe P, Blanchard C. A comparison of RS4-type resistant starch to RS2-type resistant starch in suppressing oxidative stress in high-fat-diet-induced obese rats. Food Funct. 2017; 8(1): 232-40.
 
[26]  Dhital S, Dabit L, Zhang B, Flanagan B, Shrestha AK. In vitro digestibility and physicochemical properties of milled rice. Food Chem. 2015; 172: 757-65.
 
[27]  Ghosh S, Collier A. Section 1 - Diagnosis, classification, epidemiology and biochemistry. In: Ghosh S, Collier A, editors. Churchill's Pocketbook of Diabetes. 2nd ed. Oxford: Churchill Livingstone; 2012. p. 1-49.
 
[28]  Siques P, Brito J, Naveas N, Pulido R, De la Cruz JJ, Mamani M, et al. Plasma and liver lipid profiles in rats exposed to chronic hypobaric hypoxia: changes in metabolic pathways. High Alt Med Biol. 2014; 15(3): 388-95.
 
[29]  Kim C, Vaziri ND. Down-regulation of hepatic LDL receptor-related protein (LRP) in chronic renal failure. Kidney Int. 2005; 67(3): 1028-32.
 
[30]  Li JB, Wang CY, Chen JW, Feng ZQ, Ma HT. Expression of liver insulin-like growth factor 1 gene and its serum level in patients with diabetes. World J Gastroenterol. 2004; 10(2): 255-9.
 
[31]  Ye X, Kohtz A, Pollonini G, Riccio A, Alberini CM. Insulin Like Growth Factor 2 Expression in the Rat Brain Both in Basal Condition and following Learning Predominantly Derives from the Maternal Allele. PLoS One. 2015; 10(10): e0141078.
 
[32]  Curtasu MV, Tafintseva V, Bendiks ZA, Marco ML, Kohler A, Xu Y, et al. Obesity-Related Metabolome and Gut Microbiota Profiles of Juvenile Gottingen Minipigs-Long-Term Intake of Fructose and Resistant Starch. Metabolites. 2020; 10(11).
 
[33]  Baghurst PA, Baghurst K, Record S. Dietary fibre, non-starch polysaccharides and resistant starch: a review. Food Aus. 1996; 48: S3-35.
 
[34]  Murphy MM, Douglass JS, Birkett A. Resistant starch intakes in the United States. J Am Diet Assoc. 2008; 108(1): 67-78.
 
[35]  Penn-Marshall M, Holtzman GI, Barbeau WE. African Americans may have to consume more than 12 grams a day of resistant starch to lower their risk for type 2 diabetes. Journal of medicinal food. 2010; 13(4): 999-1004.
 
[36]  Roben A, Andersen K, Karberg MA. Acetylation of or B-cyclodesetrin addition to potato starch: Beneficial effect on glucosemetabolism and appetite sensations. The American journal of clinical nutrition. 1997; 66: 304-14.
 
[37]  Bodinham CL, Frost GS, Robertson MD. Acute ingestion of resistant starch reduces food intake in healthy adults. Br J Nutr. 2010; 103(6): 917-22.
 
[38]  Ble-Castillo JL, Juarez-Rojop IE, Tovilla-Zarate CA, Garcia-Vazquez C, Servin-Cruz MZ, Rodriguez-Hernandez A, et al. Acute Consumption of Resistant Starch Reduces Food Intake but Has No Effect on Appetite Ratings in Healthy Subjects. Nutrients. 2017; 9(7).
 
[39]  Saydah S, Ballard-Barbash R, Potischman N. Association of metabolic syndrome with insulin-like growth factors among adults in the US. Cancer Causes Control. 2009; 20(8): 1309-16.
 
[40]  Pouriamehr S, Barmaki H, Rastegary M, Lotfi F, Nabi Afjadi M. Investigation of insulin-like growth factors/insulin-like growth factor binding proteins regulation in metabolic syndrome patients. BMC Res Notes. 2019; 12(1): 653.
 
[41]  Yiu WF, Kwan PL, Wong CY, Kam TS, Chiu SM, Chan SW, et al. Attenuation of fatty liver and prevention of hypercholesterolemia by extract of Curcuma longa through regulating the expression of CYP7A1, LDL-receptor, HO-1, and HMG-CoA reductase. J Food Sci. 2011; 76(3): H80-9.
 
[42]  Kunnumakkara AB, Bordoloi D, Padmavathi G, Monisha J, Roy NK, Prasad S, et al. Curcumin, the golden nutraceutical: multitargeting for multiple chronic diseases. Br J Pharmacol. 2017; 174(11): 1325-48.
 
[43]  Adab Z, Eghtesadi S, Vafa M, Heydari I, Shojaei A, Haqqani H, et al. Effect of turmeric on body measurement indices, glycemic condition, and lipid profile in hyperlipidemic patients with type 2 diabetes. Iran J Nutr Sci Food Technol. 2013; 8(3): 217-21.
 
[44]  Shehzad A, Wahid F, Lee YS. Curcumin in cancer chemoprevention: molecular targets, pharmacokinetics, bioavailability, and clinical trials. Arch Pharm (Weinheim). 2010; 343(9): 489-99.
 
[45]  Peterson CT, Rodionov DA, Iablokov SN, Pung MA, Chopra D, Mills PJ, et al. Prebiotic Potential of Culinary Spices Used to Support Digestion and Bioabsorption. Evid Based Complement Alternat Med. 2019; 2019: 8973704.
 
[46]  Martinez I, Lattimer JM, Hubach KL, Case JA, Yang J, Weber CG, et al. Gut microbiome composition is linked to whole grain-induced immunological improvements. ISME J. 2013; 7(2): 269-80.
 
[47]  De Angelis M, Ferrocino I, Calabrese FM, De Filippis F, Cavallo N, Siragusa S, et al. Diet influences the functions of the human intestinal microbiome. Sci Rep. 2020; 10(1): 4247.
 
[48]  Kostic AD, Gevers D, Siljander H, Vatanen T, Hyotylainen T, Hamalainen AM, et al. The dynamics of the human infant gut microbiome in development and in progression toward type 1 diabetes. Cell Host Microbe. 2015; 17(2): 260-73.
 
[49]  Kameyama K, Itoh K. Intestinal colonization by a Lachnospiraceae bacterium contributes to the development of diabetes in obese mice. Microbes Environ. 2014; 29(4): 427-30.
 
[50]  Dinh DM, Volpe GE, Duffalo C, Bhalchandra S, Tai AK, Kane AV, et al. Intestinal microbiota, microbial translocation, and systemic inflammation in chronic HIV infection. J Infect Dis. 2015; 211(1): 19-27.
 
[51]  Palm NW, de Zoete MR, Cullen TW, Barry NA, Stefanowski J, Hao L, et al. Immunoglobulin A coating identifies colitogenic bacteria in inflammatory bowel disease. Cell. 2014; 158(5): 1000-10.
 
[52]  Zhang H, DiBaise JK, Zuccolo A, Kudrna D, Braidotti M, Yu Y, et al. Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci U S A. 2009; 106(7): 2365-70.
 
[53]  Guo P, Zhang K, Ma X, He P. Clostridium species as probiotics: potentials and challenges. J Anim Sci Biotechnol. 2020; 11: 24.