Abstract
Background
Previous studies have shown thylakoids, the membrane proteins which are extracted from green leaves like spinach, can induce satiety through homeostatic and non-homeostatic pathways. In this study, we reviewed the current human literature on thylakoids’ characteristics and their relationship to satiety regulation and weight loss.
Methods
A systematic search of literature published between January 1990 and May 2019 was conducted on the electronic databases; including WEB OF SCIENCE, Cochrane Library, MEDLINE, Scopus, and EMBASE databases. We included all clinical trials that addressed the effects of thylakoids or chloroplast intake on satiety and weight loss.
Results
After excluding non-human studies, non-RCTs, duplications, studies with irrelevant data and interventions, eight studies were included in the qualitative synthesis. All studies supported this hypothesis that thylakoids reduce the feeling of hunger by increasing postprandial cholecystokinin and leptin and decreasing serum ghrelin, but the consequences of thylakoid intake on anthropometric characteristics were controversial.
Conclusion
In conclusion, our results may approve this postulation that receiving a thylakoid-enriched meal can decrease appetite and probably food intake in short term; however, more studies are needed to explore the effects of long term supplementation with thylakoids on weight loss in human subjects.
Similar content being viewed by others
References
Organization WH. Obesity: preventing and managing the global epidemic report of a WHO Consultation (WHO Technical Report Series 894)2000. 252 p.
Garrow JS. Obesity and related diseases. London: Churchill Livingstone; 1988.
(World Healtrh Organization (WHO) Obesity and Overweight, 2017 http://www.who.int/mediacentre/factsheets/fs311/en. Accessed 18 Dec 2017.
Yusuf S, Reddy S, Ounpuu S, Anand S. Global burden of cardiovascular diseases: part I: general considerations, the epidemiologic transition, risk factors, and impact of urbanization. Circulation. 2001;104(22):2746–53.
Omran AR. The epidemiologic transition: a theory of the epidemiology of population change. 1971. Milbank Q. 2005;83(4):731–57.
Hagan S, Niswender KD. Neuroendocrine regulation of food intake. Pediatr Blood Cancer. 2012;58(1):149–53.
Cummings DE, Overduin J. Gastrointestinal regulation of food intake. J Clin Invest. 2007;117(1):13–23.
Juhler RK, Andreasson E, Yu SG, Albertsson PK. Composition of photosynthetic pigments in thylakoid membrane vesicles from spinach. Photosynth Res. 1993;35(2):171–8.
Mustárdy L, Buttle K, Steinbach G, Garab G. The three-dimensional network of the thylakoid membranes in plants: quasihelical model of the granum-stroma assembly. Plant Cell. 2008;20(10):2552–7. https://doi.org/10.1105/tpc.108.059147.
Montelius C, Erlandsson D, Vitija E, Stenblom EL, Egecioglu E, Erlanson-Albertsson C. Body weight loss, reduced urge for palatable food and increased release of GLP-1 through daily supplementation with green-plant membranes for three months in overweight women. Appetite. 2014;81:295–304.
Albertsson PA, Kohnke R, Emek SC, Mei J, Rehfeld JF, Akerlund HE, et al. Chloroplast membranes retard fat digestion and induce satiety: effect of biological membranes on pancreatic lipase/co-lipase. Biochem J. 2007;401(3):727–33.
Stenblom EL, Egecioglu E, Landin-Olsson M, Erlanson-Albertsson C. Consumption of thylakoid-rich spinach extract reduces hunger, increases satiety and reduces cravings for palatable food in overweight women. Appetite. 2015;91:209–19.
Rebello CJ, Chu J, Beyl R, Edwall D, Erlanson-Albertsson C, Greenway FL. Acute effects of a spinach extract rich in thylakoids on satiety: a randomized controlled crossover trial. J Am Coll Nutr. 2015;34(6):470–7.
Montelius C, Osman N, Westrom B, Ahrne S, Molin G, Albertsson PA, et al. Feeding spinach thylakoids to rats modulates the gut microbiota, decreases food intake and affects the insulin response. J Nutr Sci. 2013;24:2.
Blaut M. Gut microbiota and energy balance: role in obesity. Proc Nutr Soc. 2015 Aug;74(3):227–34. https://doi.org/10.1017/S0029665114001700.
Villanueva-Millan MJ, Perez-Matute P, Oteo JA. Gut microbiota: a key player in health and disease. A review focused on obesity. J Physiol Biochem. 2015;71(3):509–25.
Erlanson-Albertsson C, Albertsson PA. The use of green leaf membranes to promote appetite control, suppress hedonic hunger and loose body weight. Plant Foods Hum Nutr. 2015;70(3):281–90.
Stenblom E-L, Montelius C, Erlandsson D, Skarping L, Fransson M, Egecioglu E, et al. Decreased urge for palatable food after a two-month dietary intervention with green-plant membranes in overweight women. J Obes Weight Loss Ther. 2014;4:8.
Stenblom EL, Montelius C, Ostbring K, Hakansson M, Nilsson S, Rehfeld JF, et al. Supplementation by thylakoids to a high carbohydrate meal decreases feelings of hunger, elevates CCK levels and prevents postprandial hypoglycaemia in overweight women. Appetite. 2013;68:118–23.
Kohnke R, Lindbo A, Larsson T, Lindqvist A, Rayner M, Emek SC, et al. Thylakoids promote release of the satiety hormone cholecystokinin while reducing insulin in healthy humans. Scand J Gastroenterol. 2009;44(6):712–9.
Maruyama C, Kikuchi N, Masuya Y, Hirota S, Araki R, Maruyama T. Effects of green-leafy vegetable intake on postprandial glycemic and lipidemic responses and alpha-tocopherol concentration in normal weight and obese men. J Nutr Sci Vitaminol. 2013;59(4):264–71.
Stenblom E-L, Weström B, Linninge C, Bonn P, Farrell M, Rehfeld JF, et al. Dietary green-plant thylakoids decrease gastric emptying and gut transit, promote changes in the gut microbial flora, but does not cause steatorrhea. Nutr Metab. 2016;13(1):67.
Emek SC, Akerlund HE, Erlanson-Albertsson C, Albertsson PA. Pancreatic lipase-colipase binds strongly to the thylakoid membrane surface. J Sci Food Agric. 2013;93(9):2254–8.
Ostbring K, Rayner M, Sjoholm I, Otterstrom J, Albertsson PA, Emek SC, et al. The effect of heat treatment of thylakoids on their ability to inhibit in vitro lipase/co-lipase activity. Food Funct. 2014;5(9):2157–65.
D'Agostino D, Cordle RA, Kullman J, Erlanson-Albertsson C, Muglia LJ, Lowe ME. Decreased postnatal survival and altered body weight regulation in procolipase-deficient mice. J Biol Chem. 2002;277(9):7170–7.
Erlanson-Albertsson C, York D. Enterostatin--a peptide regulating fat intake. Obes Res. 1997;5(4):360–72.
Panda V, Shinde P. Appetite suppressing effect of Spinacia oleracea in rats: involvement of the short term satiety signal cholecystokinin. Appetite. 2017;113:224–30.
Beglinger S, Drewe J, Schirra J, Goke B, D'Amato M, Beglinger C. Role of fat hydrolysis in regulating glucagon-like Peptide-1 secretion. J Clin Endocrinol Metab. 2010;95(2):879–86.
Dockray GJ. Gastrointestinal hormones and the dialogue between gut and brain. J Physiol. 2014;592(14):2927–41.
Nauck MA, Niedereichholz U, Ettler R, Holst JJ, Orskov C, Ritzel R, et al. Glucagon-like peptide 1 inhibition of gastric emptying outweighs its insulinotropic effects in healthy humans. Am J Phys. 1997;273(5 Pt 1):E981–8.
Kirchner H, Heppner KM, Tschop MH. The role of ghrelin in the control of energy balance. Handb Exp Pharmacol. 2012;209:161–84.
Degen L, Drewe J, Piccoli F, Grani K, Oesch S, Bunea R, et al. Effect of CCK-1 receptor blockade on ghrelin and PYY secretion in men. Am J Physiol Regul Integr Comp Physiol. 2007;292(4):30.
Pelleymounter MA, Cullen MJ, Baker MB, Hecht R, Winters D, Boone T, et al. Effects of the obese gene product on body weight regulation in Ob/Ob mice. Science. 1995;269(5223):540–3.
Blundell JE, Gillett A. Control of food intake in the obese. Obes Res. 2001;9(4):129.
Kondo S, Xiao JZ, Satoh T, Odamaki T, Takahashi S, Sugahara H, et al. Antiobesity effects of Bifidobacterium breve strain B-3 supplementation in a mouse model with high-fat diet-induced obesity. Biosci Biotechnol Biochem. 2010;74(8):1656–61.
Hardikar AA. Role of incretins in pancreas growth and development. JOP. 2004 Nov 10;5(6):454–6.
Lowe MR, Butryn ML. Hedonic hunger: a new dimension of appetite? Physiol Behav. 2007;91(4):432–9.
Egecioglu E, Jerlhag E, Salome N, Skibicka KP, Haage D, Bohlooly YM, et al. Ghrelin increases intake of rewarding food in rodents. Addict Biol. 2010;15(3):304–11.
Skibicka KP. The central GLP-1: implications for food and drug reward. Front Neurosci. 2013;7(181):00181.
Yamaguchi E, Yasoshima Y, Shimura T. Systemic administration of anorexic gut peptide hormones impairs hedonic-driven sucrose consumption in mice. Physiol Behav. 2017;171:158–64.
Figlewicz DP, Benoit SC. Insulin, leptin, and food reward: update 2008. Am J Physiol Regul Integr Comp Physiol. 2009;296(1):R9–R19.
Kohnke R, Lindqvist A, Goransson N, Emek SC, Albertsson PA, Rehfeld JF, et al. Thylakoids suppress appetite by increasing cholecystokinin resulting in lower food intake and body weight in high-fat fed mice. Phytother Res. 2009;23(12):1778–83.
Stenkula KG, Stenblom EL, Montelius C, Egecioglu E, Erlanson-Albertsson C. Thylakoids reduce body fat and fat cell size by binding to dietary fat making it less available for absorption in high-fat fed mice. Nutr Metab. 2017;14(4):016–0160.
Tagliabue A, Elli M. The role of gut microbiota in human obesity: recent findings and future perspectives. Nutr Metab Cardiovasc Dis. 2013;23(3):160–8.
Tehrani AB, Nezami BG, Gewirtz A, Srinivasan S. Obesity and its associated disease: a role for microbiota? Neurogastroenterol Motil. 2012;24(4):305–11.
Cani PD, Geurts L, Matamoros S, Plovier H, Duparc T. Glucose metabolism: focus on gut microbiota, the endocannabinoid system and beyond. Diabetes Metab. 2014;40(4):246–57.
Moya-Perez A, Neef A, Sanz Y. Bifidobacterium pseudocatenulatum CECT 7765 reduces obesity-associated inflammation by restoring the lymphocyte-macrophage balance and gut microbiota structure in high-fat diet-fed mice. PLoS One. 2015;10(7):e0126976.
Cano PG, Santacruz A, Trejo FM, Sanz Y. Bifidobacterium CECT 7765 improves metabolic and immunological alterations associated with obesity in high-fat diet-fed mice. Obesity. 2013;21(11):2310–21.
Million M, Angelakis E, Paul M, Armougom F, Leibovici L, Raoult D. Comparative meta-analysis of the effect of Lactobacillus species on weight gain in humans and animals. Microb Pathog. 2012;53(2):100–8.
Fak F, Backhed F. Lactobacillus reuteri prevents diet-induced obesity, but not atherosclerosis, in a strain dependent fashion in Apoe−/− mice. PLoS One. 2012;7(10):9.
Kaji I, Karaki S, Kuwahara A. Short-chain fatty acid receptor and its contribution to glucagon-like peptide-1 release. Digestion. 2014;89(1):31–6.
den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud DJ, Bakker BM. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res. 2013;54(9):2325–40.
Funding
This study was supported by Student Research Committee, Iran University of Medical Sciences (IUMS), Tehran, Iran.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflicts of interest to declare.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOC 82 kb)
Rights and permissions
About this article
Cite this article
Amirinejad, A., Heshmati, J. & Shidfar, F. Effects of thylakoid intake on appetite and weight loss: a systematic review. J Diabetes Metab Disord 19, 565–573 (2020). https://doi.org/10.1007/s40200-019-00443-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40200-019-00443-w