Korean Journal of Community Nutrition (대한지역사회영양학회지)

The Korean Society of Community Nutrition (대한지역사회영양학회)
권호 표지
DOI QR코드

DOI QR Code

Effects of natural mono- and di-saccharide as alternative sweeteners on inflammatory bowel disease: a narrative review

  • Eunju Kim (Department of Biochemistry and Molecular Biology, McGovern Medical School, The University of Texas Health Science Center at Houston)
  • Received : 2023.06.01
  • Accepted : 2023.06.24
  • Published : 2023.06.30
Download PDF
⟨ Previous Next ⟩

Abstract

Objectives: The incidence of inflammatory bowel disease (IBD) is increasing globally, and excessive added sugar consumption has been identified as one of the contributing factors. In the context of IBD, it is essential to explore functional sweeteners that can improve metabolic health and minimize the risk of IBD-related symptoms. This review article aims to shed light on the effects of natural mono- and di-saccharides as alternative sweeteners, specifically focusing on potential benefits for IBD. Methods: A comprehensive literature review was performed using PubMed and Google Scholar databases with articles published after the year 2000. The search terms 'IBD', 'added sugar', 'sweeteners', 'mono-saccharide', and 'di-saccharide' were combined to retrieve relevant articles. A total of 21 manuscripts, aligning with the objectives of the study, were selected. Papers focusing on artificial or high-intensity sweeteners were excluded to ensure relevant literature selection. Results: Multiple studies have emphasized the association between the high consumption of added sugars such as simple sugars and the increased risk of developing IBD. This is suggested to be attributed to the induction of pro-inflammatory cytokine productions and dysbiosis of the gut microbiota. Consequently, there is a growing demand for safe and functional sweeteners, in particular mono- and di-saccharides, that can serve as alternatives for IBD patients. Those functional sweeteners regulate inflammation, oxidative stress, and Intestinal barrier protection, and restore microbiome profiles in various IBD models including cells, animals, and humans. Conclusions: Understanding these mechanisms resolves the link between how sugar consumption and IBD, and highlights the beneficial effects of natural alternative sweeteners on IBD when they were administered by itself or as a replacement for simple sugar. Further, exploration of this relationship leads us to recognize the necessity of natural alternative sweeteners in dietary planning. This knowledge could potentially lead to more effective dietary strategies for individuals with IBD.

Keywords

References

  1. Veauthier B, Hornecker JR. Crohn's disease: Diagnosis and management. Am Fam Physician 2018; 98(11): 661-669.
  2. Kaplan GG, Windsor JW. The four epidemiological stages in the global evolution of inflammatory bowel disease. Nat Rev Gastroenterol Hepatol 2021; 18(1): 56-66. https://doi.org/10.1038/s41575-020-00360-x
  3. Burisch J, Munkholm P. Inflammatory bowel disease epidemiology. Curr Opin Gastroenterol 2013; 29(4): 357-362. https://doi.org/10.1097/MOG.0b013e32836229fb
  4. Burisch J, Munkholm P. The epidemiology of inflammatory bowel disease. Scand J Gastroenterol 2015; 50(8): 942-951. https://doi.org/10.3109/00365521.2015.1014407
  5. Shin SH. The trend of treating inflammatory bowel disease in the last 10 years [Internet]. Health Insurance Review & Assessment Service; 2020 [cited 2023 May 5]. Available from: https://repository.hira.or.kr/handle/2019.oak/2305.
  6. Seyedian SS, Nokhostin F, Malamir MD. A review of the diagnosis, prevention, and treatment methods of inflammatory bowel disease. J Med Life 2019; 12(2): 113.
  7. Chen L, Deng H, Cui H, Fang J, Zuo Z, Deng J et al. Inflammatory responses and inflammation-associated diseases in organs. Oncotarget 2018; 9(6): 7204.
  8. Strober W, Fuss I, Mannon P. The fundamental basis of inflammatory bowel disease. J Clin Invest 2007; 117(3): 514-521. https://doi.org/10.1172/JCI30587
  9. Arnone D, Chabot C, Heba AC, Kokten T, Caron B, Hansmannel F et al. Sugars and gastrointestinal health. Clin Gastroenterol Hepatol 2022; 20(9): 1912-1924. https://doi.org/10.1016/j.cgh.2021.12.011
  10. Stanhope KL. Sugar consumption, metabolic disease and obesity: The state of the controversy. Crit Rev Clin Lab Sci 2016; 53(1): 52-67. https://doi.org/10.3109/10408363.2015.1084990
  11. Food and Drug Administration. Added sugars on the new nutrition facts label [Internet]. Food and Drug Administration; 2022 [cited 2023 May 7]. Available from: https://www.fda.gov/food/new-nutrition-facts-label/added-sugars-new-nutrition-facts-label#:~:text=The%20Dietary%20Guidelines%20for%20Americans,of%20added%20sugars%20per%20day.
  12. Hou JK, Abraham B, El-Serag H. Dietary intake and risk of developing inflammatory bowel disease: A systematic review of the literature. Am J Gastroenterol 2011; 106(4): 563-573. https://doi.org/10.1038/ajg.2011.44
  13. Racine A, Carbonnel F, Chan SS, Hart AR, Bueno-de-Mesquita HB, Oldenburg B et al. Dietary patterns and risk of inflammatory bowel disease in Europe: Results from the EPIC study. Inflamm Bowel Dis 2016; 22(2): 345-354. https://doi.org/10.1097/MIB.0000000000000638
  14. Khan S, Waliullah S, Godfrey V, Khan MAW, Ramachandran RA, Cantarel BL et al. Dietary simple sugars alter microbial ecology in the gut and promote colitis in mice. Sci Transl Med 2020; 12(567): eaay6218.
  15. Kalantar-Zadeh K, Berean KJ, Burgell RE, Muir JG, Gibson PR. Intestinal gases: Influence on gut disorders and the role of dietary manipulations. Nat Rev Gastroenterol Hepatol 2019; 16(12): 733-747. https://doi.org/10.1038/s41575-019-0193-z
  16. Yu Y, Shen M, Song Q, Xie J. Biological activities and pharmaceutical applications of polysaccharide from natural resources: A review. Carbohydr Polym 2018; 183: 91-101. https://doi.org/10.1016/j.carbpol.2017.12.009
  17. Niu W, Chen X, Xu R, Dong H, Yang F, Wang Y et al. Polysaccharides from natural resources exhibit great potential in the treatment of ulcerative colitis: A review. Carbohydr Polym 2021; 254: 117189.
  18. Saraiva A, Carrascosa C, Raheem D, Ramos F, Raposo A. Natural sweeteners: The relevance of food naturalness for consumers, food security aspects, sustainability and health impacts. Int J Environ Res Public Health 2020; 17: 6285.
  19. Paterson HM, Murphy TJ, Purcell EJ, Shelley O, Kriynovich SJ, Lien E et al. Injury primes the innate immune system for enhanced Toll-like receptor reactivity. J Immunol 2003; 171(3): 1473-1483. https://doi.org/10.4049/jimmunol.171.3.1473
  20. Wallace JL. COX-2: A pivotal enzyme in mucosal protection and resolution of inflammation. Sci World J 2006; 6: 577-588. https://doi.org/10.1100/tsw.2006.122
  21. Avdagic N, Zaciragic A, Babic N, Hukic M, Seremet M, Lepara O et al. Nitric oxide as a potential biomarker in inflammatory bowel disease. Bosn J Basic Med Sci 2013; 13(1): 5.
  22. Jablonski KA, Amici SA, Webb LM, de Dios Ruiz-Rosado J, Popovich PG, Partida-Sanchez S et al. Novel markers to delineate murine M1 and M2 macrophages. PLoS One 2015; 10(12): e0145342.
  23. Nishida A, Inoue R, Inatomi O, Bamba S, Naito Y, Andoh A. Gut microbiota in the pathogenesis of inflammatory bowel disease. Clin J Gastroenterol 2018; 11(1): 1-10. https://doi.org/10.1007/s12328-017-0813-5
  24. Thoreson R, Cullen JJ. Pathophysiology of inflammatory bowel disease: An overview. Surg Clin North Am 2007; 87(3): 575-585. https://doi.org/10.1016/j.suc.2007.03.001
  25. Bowman SA. Added sugars: Definition and estimation in the USDA Food Patterns Equivalents Databases. J Food Compost Anal 2017; 64: 64-67. https://doi.org/10.1016/j.jfca.2017.07.013
  26. Niaz K, Khan F, Shah MA. Analysis of carbohydrates (monosaccharides, polysaccharides). In: Sanches Silva A, Nabavi SF, Saeedi M. and Nabavi SM, editors. Recent advances in natural products analysis. : Elsevier press; 2020. p. 621-633.
  27. Van Horn L, Carson JAS, Appel LJ, Burke LE, Economos C, Karmally W et al. Recommended dietary pattern to achieve adherence to the American Heart Association/American College of Cardiology (AHA/ACC) guidelines: A scientific statement from the American Heart Association. Circulation 2016; 134(22): e505-e529. https://doi.org/10.1161/CIR.0000000000000462
  28. USDA, Economics Research Service. Sugar and sweeteners yearbook tables [Internet]. Economics Research Service. USDA; 2018 [cited 2023 May 9]. Available from: https://www.ers.usda.gov/data-products/sugar-and-sweeteners-yearbook-tables.aspx. Accessed, 3.
  29. Korea Disease Control and Prevention Agency. The daily dietary sugar intake in Korea [Internet]. Korea Disease Control and Prevention Agency; 2018 [cited 2023 May 11]. Available from: https://www.kdca.go.kr/.
  30. Lee HS, Kwon SO, Yon M, Kim D, Lee JY, Nam J et al. Dietary total sugar intake of Koreans: Based on the Korea National Health and Nutrition Examination Survey (KNHANES), 2008-2011. J Nutr Health 2014; 47(4): 268-276. https://doi.org/10.4163/jnh.2014.47.4.268
  31. Holt DJ, Chamberlain LM, Grainger DW. Cell-cell signaling in co-cultures of macrophages and fibroblasts. Biomaterials 2010; 31(36): 9382-9394. https://doi.org/10.1016/j.biomaterials.2010.07.101
  32. Wang L, Ji T, Yuan Y, Fu H, Wang Y, Tian S et al. High-fructose corn syrup promotes proinflammatory Macrophage activation via ROS-mediated NF-κB signaling and exacerbates colitis in mice. Int Immunopharmacol 2022; 109: 108814.
  33. Laffin M, Fedorak R, Zalasky A, Park H, Gill A, Agrawal A et al. A high-sugar diet rapidly enhances susceptibility to colitis via depletion of luminal short-chain fatty acids in mice. Sci Rep 2019; 9(1): 12294.
  34. Han MK, Anderson R, Viennois E, Merlin D. Examination of food consumption in United States adults and the prevalence of inflammatory bowel disease using National Health Interview Survey 2015. PLoS One 2020; 15(4): e0232157.
  35. Martinez KB, Leone V, Chang EB. Western diets, gut dysbiosis, and metabolic diseases: Are they linked? Gut Microbes 2017; 8(2): 130-142. https://doi.org/10.1080/19490976.2016.1270811
  36. Sun S, Araki Y, Hanzawa F, Umeki M, Kojima T, Nishimura N et al. High sucrose diet-induced dysbiosis of gut microbiota promotes fatty liver and hyperlipidemia in rats. J Nutr Biochem 2021; 93: 108621.
  37. Wang Y, Qi W, Song G, Pang S, Peng Z, Li Y et al. High-fructose diet increases inflammatory cytokines and alters gut microbiota composition in rats. Mediators inflamm 2020; 6672636.
  38. Kotake T, Yamanashi Y, Imaizumi C, Tsumuraya Y. Metabolism of L-arabinose in plants. J Plant Res 2016; 129: 781-792. https://doi.org/10.1007/s10265-016-0834-z
  39. Li Y, Pan H, Liu JX, Li T, Liu S, Shi W et al. L-Arabinose inhibits colitis by modulating gut microbiota in mice. J Agric Food Chem 2019; 67(48): 13299-13306. https://doi.org/10.1021/acs.jafc.9b05829
  40. Kaats GR, Keith SC, Keith PL, Leckie RB, Perricone NV, Preuss HG. A combination of l-arabinose and chromium lowers circulating glucose and insulin levels after an acute oral sucrose challenge. Nutr J 2011; 10: 1-6. https://doi.org/10.1186/1475-2891-10-1
  41. Tamura M, Kurusu Y, Hori S. Effect of dietary l-arabinose on the intestinal microbiota and metabolism of dietary daidzein in adult mice. Biosci Microbiota Food Health 2012; 31(3): 59-65. https://doi.org/10.12938/bmfh.31.59
  42. Arya A, Kumar A. Teaching structural diversity of hexoses to graduate and postgraduate students: Methods to correlate stereochemistry. Biochem Mol Biol Educ 2020; 48(1): 8-20. https://doi.org/10.1002/bmb.21305
  43. Sharma V, Smolin J, Nayak J, Ayala JE, Scott DA, Peterson SN et al. Mannose alters gut microbiome, prevents diet-induced obesity, and improves host metabolism. Cell Rep 2018; 24(12): 3087-3098. https://doi.org/10.1016/j.celrep.2018.08.064
  44. Dong L, Xie J, Wang Y, Jiang H, Chen K, Li D et al. Mannose ameliorates experimental colitis by protecting intestinal barrier integrity. Nat Commun 2022; 13(1): 4804.
  45. Choi SS, Lynch BS, Baldwin N, Dakoulas EW, Roy S, Moore C et al. Safety evaluation of the human-identical milk monosaccharide, l-fucose. Regul Toxicol Pharmacol 2015; 72(1): 39-48. https://doi.org/10.1016/j.yrtph.2015.02.016
  46. Newburg DS, Ruiz-Palacios GM, Altaye M, Chaturvedi P, Meinzen-Derr J, Guerrero MdL et al. Innate protection conferred by fucosylated oligosaccharides of human milk against diarrhea in breastfed infants. Glycobiology 2004; 14(3): 253-263. https://doi.org/10.1093/glycob/cwh020
  47. He R, Li Y, Han C, Lin R, Qian W, Hou X. L-Fucose ameliorates DSS-induced acute colitis via inhibiting macrophage M1 polarization and inhibiting NLRP3 inflammasome and NF-kB activation. Int Immunopharmacol 2019; 73: 379-388. https://doi.org/10.1016/j.intimp.2019.05.013
  48. Elias PS, Benecke H, Schwengers D. Safety evaluation studies of leucrose. J Am Coll Toxicol 1996; 15(3): 205-218. https://doi.org/10.3109/10915819609008714
  49. Ziesenitz SC, Siebert G, Schwengers D, Lemmes R. Nutritional assessment in humans and rats of leucrose [D-glucopyranosyl-alpha(1----5)-D-fructopyranose] as a sugar substitute. J Nutr 1989; 119(7): 971-978. https://doi.org/10.1093/jn/119.7.971
  50. Kim E, Kim Y, Lee J, Shin JH, Seok PR, Kim Y et al. Leucrose, a natural sucrose isomer, suppresses dextran sulfate sodium (DSS)-induced colitis in mice by regulating macrophage polarization via JAK1/STAT6 signaling. J Funct Foods 2020; 74: 104156.
  51. White Jr JW, Hoban N. Composition of honey. IV. Identification of the disaccharides. Arch Biochem Biophys 1959; 80(2): 386-392. https://doi.org/10.1016/0003-9861(59)90267-X
  52. Ruiz-Aceituno L, Hernandez-Hernandez O, Kolida S, Moreno FJ, Methven L. Sweetness and sensory properties of commercial and novel oligosaccharides of prebiotic potential. LWT 2018; 97: 476-482. https://doi.org/10.1016/j.lwt.2018.07.038
  53. Chung JY, Lee J, Lee D, Kim E, Shin JH, Seok PR et al. Acute and 13-week subchronic toxicological evaluations of turanose in mice. Nutr Res Pract 2017; 11(6): 452-460. https://doi.org/10.4162/nrp.2017.11.6.452
  54. Chung JY, Kim YS, Kim Y, Yoo SH. Regulation of inflammation by sucrose isomer, turanose, in raw 264.7 cells. J Cancer Prev 2017; 22(3): 195.
  55. Sheedy FJ. Turning 21: Induction of miR-21 as a key switch in the inflammatory response. Front Immunol 2015; 6: 19.
  56. Tafere DA. Chemical composition and uses of Honey: A Review. J Food Sci Nutr Res 2021; 4(3): 194-201.
  57. Prakash A, Medhi B, Avti P, Saikia U, Pandhi P, Khanduja K. Effect of different doses of Manuka honey in experimentally induced inflammatory bowel disease in rats. Phytother Res 2008; 22(11): 1511-1519. https://doi.org/10.1002/ptr.2523
  58. Zhao H, Cheng N, Zhou W, Chen S, Wang Q, Gao H et al. Honey polyphenols ameliorate DSS-induced ulcerative colitis via modulating gut microbiota in rats. Mol Nutr Food Res 2019; 63(23): 1900638.