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Effects of thylakoid intake on appetite and weight loss: a systematic review

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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.

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References

  1. Organization WH. Obesity: preventing and managing the global epidemic report of a WHO Consultation (WHO Technical Report Series 894)2000. 252 p.

  2. Garrow JS. Obesity and related diseases. London: Churchill Livingstone; 1988.

    Google Scholar 

  3. (World Healtrh Organization (WHO) Obesity and Overweight, 2017 http://www.who.int/mediacentre/factsheets/fs311/en. Accessed 18 Dec 2017.

  4. 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.

    Article  CAS  PubMed  Google Scholar 

  5. Omran AR. The epidemiologic transition: a theory of the epidemiology of population change. 1971. Milbank Q. 2005;83(4):731–57.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Hagan S, Niswender KD. Neuroendocrine regulation of food intake. Pediatr Blood Cancer. 2012;58(1):149–53.

    Article  PubMed  Google Scholar 

  7. Cummings DE, Overduin J. Gastrointestinal regulation of food intake. J Clin Invest. 2007;117(1):13–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. 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.

    Article  CAS  PubMed  Google Scholar 

  9. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. 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.

    Article  PubMed  Google Scholar 

  11. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. 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.

    Article  PubMed  Google Scholar 

  13. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. 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.

    Google Scholar 

  15. 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.

    Article  CAS  PubMed  Google Scholar 

  16. 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.

    Article  CAS  PubMed  Google Scholar 

  17. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. 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.

    Google Scholar 

  19. 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.

    Article  PubMed  Google Scholar 

  20. 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.

    Article  CAS  PubMed  Google Scholar 

  21. 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.

    Article  CAS  PubMed  Google Scholar 

  22. 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.

    Article  CAS  Google Scholar 

  23. 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.

    Article  CAS  PubMed  Google Scholar 

  24. 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.

    Article  PubMed  CAS  Google Scholar 

  25. 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.

    Article  CAS  PubMed  Google Scholar 

  26. Erlanson-Albertsson C, York D. Enterostatin--a peptide regulating fat intake. Obes Res. 1997;5(4):360–72.

    Article  CAS  PubMed  Google Scholar 

  27. 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.

    Article  PubMed  Google Scholar 

  28. 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.

    Article  CAS  PubMed  Google Scholar 

  29. Dockray GJ. Gastrointestinal hormones and the dialogue between gut and brain. J Physiol. 2014;592(14):2927–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. 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.

    CAS  Google Scholar 

  31. Kirchner H, Heppner KM, Tschop MH. The role of ghrelin in the control of energy balance. Handb Exp Pharmacol. 2012;209:161–84.

    Article  CAS  Google Scholar 

  32. 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.

    Article  CAS  Google Scholar 

  33. 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.

    Article  CAS  PubMed  Google Scholar 

  34. Blundell JE, Gillett A. Control of food intake in the obese. Obes Res. 2001;9(4):129.

    Google Scholar 

  35. 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.

    Article  CAS  PubMed  Google Scholar 

  36. Hardikar AA. Role of incretins in pancreas growth and development. JOP. 2004 Nov 10;5(6):454–6.

    PubMed  Google Scholar 

  37. Lowe MR, Butryn ML. Hedonic hunger: a new dimension of appetite? Physiol Behav. 2007;91(4):432–9.

    Article  CAS  PubMed  Google Scholar 

  38. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Skibicka KP. The central GLP-1: implications for food and drug reward. Front Neurosci. 2013;7(181):00181.

    Google Scholar 

  40. 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.

    Article  CAS  PubMed  Google Scholar 

  41. Figlewicz DP, Benoit SC. Insulin, leptin, and food reward: update 2008. Am J Physiol Regul Integr Comp Physiol. 2009;296(1):R9–R19.

    Article  CAS  PubMed  Google Scholar 

  42. 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.

    Article  PubMed  CAS  Google Scholar 

  43. 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.

    Google Scholar 

  44. 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.

    Article  CAS  PubMed  Google Scholar 

  45. Tehrani AB, Nezami BG, Gewirtz A, Srinivasan S. Obesity and its associated disease: a role for microbiota? Neurogastroenterol Motil. 2012;24(4):305–11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. 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.

    Article  CAS  PubMed  Google Scholar 

  47. 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. 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.

    Article  CAS  PubMed  Google Scholar 

  49. 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.

    Article  PubMed  Google Scholar 

  50. 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.

    Article  CAS  Google Scholar 

  51. 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.

    Article  CAS  PubMed  Google Scholar 

  52. 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.

    Article  CAS  Google Scholar 

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Funding

This study was supported by Student Research Committee, Iran University of Medical Sciences (IUMS), Tehran, Iran.

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Authors and Affiliations

  1. Student Research Committee, Department of Nutrition, School of Public Health, Iran University of Medical Sciences, Tehran, Iran

    Ali Amirinejad

  2. Songhor Healthcare Center, Kermanshah University of Medical Science, Kermanshah, Iran

    Javad Heshmati

  3. Department of Nutrition, School of Public Health, Iran University of Medical Sciences, Tehran, Iran

    Farzad Shidfar

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  1. Ali Amirinejad
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  2. Javad Heshmati
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  3. Farzad Shidfar
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Correspondence to Farzad Shidfar.

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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

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