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Acta Cirurgica Brasileira

On-line version ISSN 1678-2674

Acta Cir. Bras. vol.27 no.3 São Paulo Mar. 2012

http://dx.doi.org/10.1590/S0102-86502012000300013 

13 - REVIEW ARTICLE

 

Fructo-oligosaccharide effects on blood glucose. An overview

 

Efeitos dos fruto-oligossacarídeos no controle glicêmico. Revisão

 

 

Graciana Teixeira CostaI; Sergio Botelho GuimarãesII; Helena Alves de Carvalho SampaioIII

IAssistant Professor, Nutrition Division, Federal University of Amazon (UFAM), Brazil. Acquisition and interpretation of data
IIPhD, Associate Professor, Department of Surgery, Head, Experimental Surgery Research Laboratory (LABCEX), Federal University of Ceara (UFC), Brazil. Critical review, interpretation of data, manuscript writing
IIIPhD, Master, Associate Professor, Nutrition Division, State University of Ceara, Fortaleza, Brazil. Conception, design, critical review

Correspondence

 

 


ABSTRACT

PURPOSE: To identify the current status of scientific knowledge in fructo-oligosaccharides (FOS), non-conventional sugars that play an important role in glycemia control.
METHODS: We performed a search for scientific articles in MEDLINE and LILACS databases, from January 1962 to December 2011, using English/Portuguese key words: "blood glucose/glicemia", "prebiotics/prebióticos" and "dietary fiber/fibras na dieta". From an initial number of 434 references, some repeated, 43 references published from 1962 to 2011 were included in this study. The selected texts were distributed in three topics: (1) metabolism of FOS, (2) FOS and experimental studies involving glucose and (3) human studies involving glucose and FOS.
RESULTS: Five studies have shown that the use of FOS reduces the fecal content and increases intestinal transit time. Experimental studies have shown that dietary supplementation with high doses (60 g/Kg) of propionate, a short-chain fatty acid decreased glycemia. The use of lower doses (3 g/kg) did not produce the same results. Study in subjects with diabetes type II showed that the addition of 8 grams of FOS in the diet for 14 days, caused a reduction in serum glucose. In another study with healthy subjects, there were no changes in glycemic control.
CONCLUSIONS: This review demonstrates that consumption of FOS has a beneficial influence on glucose metabolism. The controversies appear to be due to inadequate methodological designs and/or the small number of individuals included in some studies.

Key words: Review. Blood Glucose. Oligosaccharides. Prebiotics. Dietary Fiber.


RESUMO

OBJETIVO: Conhecer o estado atual do conhecimento científico em fructooligossacarídeos (FOS), açúcares não-convencionais que desempenham um papel importante no controle da glicemia.
MÉTODOS: Realizamos uma busca de artigos científicos nas bases de dados MEDLINE e Literatura Latino-Americana e do Caribe em Ciências da Saúde (LILACS), a partir de janeiro 1962 a dezembro de 2011, usando como descritores termos Português/Inglês: "glicemia/blood glucose, "prebióticos/prebiotics" e "fibras na dieta/dietary fiber. A partir de um número inicial de 434 referências, algumas repetidas, 43 referências foram consideradas adequadas para a finalidade deste estudo e foram, portanto, selecionadas para análise. Os textos selecionados foram distribuídos em três tópicos: (1) metabolismo de FOS (2), FOS e estudos experimentais envolvendo glicose e (3) estudos em humanos envolvendo glicose e FOS.
RESULTADOS: Cinco trabalhos mostraram que o uso de FOS diminui o conteúdo fecal e aumenta o tempo do transito intestinal. Estudos experimentais demonstraram que a suplementação dietética com altas doses (60 g/Kg) de propionato, um ácido graxo de cadeia curta, diminuiu a glicemia. A utilização de doses menores (3 g/Kg) não produziu os mesmos resultados. Em indivíduos diabéticos tipo II a adição de 8 g de FOS na dieta, durante 14 dias, induziu uma redução da glicemia. Em indivíduos sadios, não ocorreram alterações da glicemia.
CONCLUSÕES: Essa revisão mostra que o consumo de FOS exerce influência benéfica no metabolismo glicêmico. As controvérsias evidenciadas parecem estar mais ligadas a desenhos metodológicos inadequados e/ou ao número reduzido de indivíduos incluídos em alguns estudos.

Descritores: Revisão. Glicemia. Oligossacarídeos. Prebióticos. Fibras na Dieta.


 

 

Introduction

Different from the majority of simple sugars and oligosaccharides, fructo-oligosaccharide (FOS), a naturally occurring oligosaccharide, passes intact through the upper digestive tract without being digested but is degraded in the colon by indigenous bacteria1. FOS are mainly known for its ability to improve host health as it stimulates the growth of some beneficial bacteria, such as the bifidobacteria.FOS may be found in many plant foods such as bananas, onions, garlic, asparagus, wheat, rye, Jerusalem artichoke. Besides, it may be produced enzymatically6.It is possible to find industrial products containing FOS, alone or with other ingredients in Brazil. Recent use of FOS as a food ingredient has stimulated much research to know its functionality and its effects on human health, especially in relation to its bifidogenic character7. Thus, its potentially beneficial effects in preventing and controlling some diseases have been extensively discussed, particularly in those conditions associated with the increase of peripheral insulin resistance, eg, diabetes mellitus and metabolic syndrome.Recent studies suggest that butyrate and other short-chain fatty acids (SCFA) may mediate the effects of diet and gut microbiota on host appetite, metabolism, adiposity, and immunity8-11.

Considering that non digestible oligosaccharides are often cited as being important dietary fibers in nutritional advice concerning specific disorders associated with the metabolic syndrome12, the aim of this review was to know the current status of FOS specific role in blood glucose control.

 

Methods

We conducted a search for scientific articles in MEDLINE and Latin American Literature and Caribbean in Health Sciences (LILACS) databases, from January 1962 to December 2011, using English/Portuguese keywords: "blood glucose/glicemia", "prebiotics/prebióticos" and "dietary fiber/fibras na dieta". From an initial number of 434 references, some repeated, 43 references published from January1962 to December 2011 were included in this study. The selected texts were distributed in three topics: (1) metabolism of FOS, (2) FOS and experimental studies involving glucose and (3) human studies involving glucose and FOS.

 

Results

Metabolism of FOS

FOS are not hydrolyzed by endogenous enzymes in the small intestine of humans and following ingestion reach the cecum and colon in intact form, where they are metabolized completely by the colonic microflora, through fermentation, producing gases (carbon dioxide, hydrogen, methane) and reducing the colon pH by lactate and SCFA production, such as acetate, propionate and butyrate, which are quickly absorbed by the colonic mucosa13-17.The solubility of these oligosaccharides in water decreases fecal content and increases intestinal transit time Butyrate, together with acetate and propionate, are major SCFA, also known as volatile fatty acids, produced by microbial fermentation in the gastrointestinal tract18.

Digestive tolerance to FOS depends on the amount ingested, the presence of factors that reduce their osmotic load in the small intestine and the degree of adaptation of the colonic microflora in the fermentation of these sugars. The osmotic effect of these sugars is determined by the concentration of sugar that leaves the stomach and this obviously depends on the amount ingested, but also on factors that slow gastric emptying, the type of meal and its solid content and viscosity16. The fraction fermented in the large intestine provides 8.4 kJ / g (2 kcal) and energy loss when a sugar is fermented is approximately 50%16.

Experimental studies

Boillot et al.19 showed that long-term dietary supplementation with propionate lowers blood glucose, suggesting that the improvement in glucose tolerance and insulin sensitivity may be due to propionate effects on carbohydrate metabolism. A study using Sprague-Dawley rats showed that these concentrations were not affected by supplemental propionate, a short-chain fatty acid. However, it should be noted that the amount of propionate in this study was small (3g / kg), compared with the previous study, where twenty-fold larger doses were used20. Although it is known that high levels of free fatty acids (FFA) are associated with insensitivity to insulin and inhibition of glucose uptake by muscle21, some studies have found that lower FFA levels were not associated with a reduction in blood glucose, although in fasting, such levels have shown a tendency to lower values in the group fed with propionate but no significant difference between groups19.

Propionate has some hypoglycemic effect under certain circumstances22. The mechanism of action of propionate at cellular level in isolated rat hepatocytes23 is related to a decrease in gluconeogenesis24, inhibition of pyruvate carboxylase, which in turn is inhibited by metabolic products of propionate, the methylmalonyl-CoA and succinyl CoA25. In addition, propionate stimulates glycolysis in isolated rat hepatocytes24 although shown to be gluconeogenic in vitro23.

Clinical studies

Yamashita et al.26 studied the systemic effects of adding FOS (8g daily) for 14 days to the diet of patients with type 2 diabetes mellitus whose serum glucose concentration was uncontrolled. Fasting blood test showed an 8% reduction in serum glucose levels26. Alles et al.6 used 15g for 20 days in patients with type 2 diabetes and found no significant changes in glucose levels. In another study, Luo et al.27 showed that chronic consumption of 20 g FOS / day in healthy individuals decreased the hepatic glucose production but had no effect on glucose metabolism stimulated by insulin. Similar results were found by other researchers28,29.Parnell and Reimer30 studied the effects of oligofructose supplementation on body weight and satiety hormone concentrations in adults and concluded that oligofructose supplementation has the potential to promote weight loss and improve glucose regulation in overweight adults. Published studies have demonstrated that consumption of foods containing the soluble ûber, b-glucan from oats and barley, have beneûcial effects on glucose metabolism, lipids and blood pressure in overweight and/or mildly hypercholesterolemic persons31. De Mello and Laaksonen studied the effects of dietary fiber in the treatment of metabolic syndrome and type 2 diabetes mellitus. After an extensive literature review the authors concluded that, despite the paucity of data on longer-term studies that focus specifically on dietary fiber, the recommended use of 25g of fiber per day from a diet rich in whole grains, fruits and vegetables, is likely to decrease the risk for obesity, metabolic syndrome and type 2 diabetes mellitus32.

Acetate can reduce plasma free fatty acids (FFA)33 and this could benefit the blood glucose and insulin sensitivity in the long term because high concentrations of fatty acids decrease tissue glucose utilization and increase tissue insulin resistance21.Unlike sucrose, 25g of FOS did not increase serum levels of postprandial glucose and fructose16. The improvement in carbohydrate metabolism could be justified by the SCFA, since propionate and / or acetate administered intravenously, orally or by rectal infusion reduces plasma FFA concentrations34,35. For Cummings36, SCFA absorbed in the colon can improve carbohydrate metabolism, considering that a high concentration of sodium propionate in the diet is associated with a noticeable improvement in carbohydrate tolerance due to inhibition of salivary amylase. Other studies where viscous fiber meals and low glycemic index foods37,38 replaced the normal diet in healthy volunteers39 and in patients with diabetes40,41also indicated a subsequent reduction in the concentrations of blood glucose and insulin. However, Giacco et al.42, using FOS 10.6 g /day of did not detect effects on blood glucose, either in fasting or in the postprandial period.Studies with infants indicate that consumption of prebiotic mixtures galactooligosaccharide / fructooligosaccharide and inulin/ galactooligosaccharide reduce the incidence of infections43. These results are important, especially in the preparation of infant formula, although these studies are not conclusive with respect to diarrhea, especially in patients with chronic intestinal inflammation and those in treatment with antibiotics. In general, dietary fiber and FOS appear to have similar effects in children and adults.

 

Conclusions

This review demonstrates that consumption of FOS has a beneficial influence on glucose metabolism. The controversies verified here seem to be linked to inadequate methodological designs and/or the small number of individuals included in some studies. The use of FOS supplementation in the diet may therefore be a strategy for reducing blood glucose. The duration of the treatment and dose to be administered are still questions to be answered. Further studies may clarify these questionings.

 

References

1. McIntyre A, Young GP, Taranto T, Gibson PR,Ward PB. Different fibers have different regional effects on luminal contents of rat colon. Gastroenterology. 1991;101(5):1274-81.         [ Links ]

2. Gibson GR, Beatty ER, Wang X, Cummings JH. Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. Gastroenterology. 1995;108:975-82.         [ Links ]

3. Blaut M. Relationship of prebiotics and food to intestinal microflora. Eur J Nutr. 2002;41 Suppl 1:11-6.         [ Links ]

4. Sartor RB. Therapeutic manipulation of the enteric microflora in inflammatory bowel diseases: antibiotics, probiotics, and prebiotics. Gastroenterology. 2004;126:1620-33.         [ Links ]

5. Macfarlane S, Macfarlane GT, Cummings JH. Review article: prebiotics in the gastrointestinal tract. Aliment Pharmacol Ther. 2006;24:701-14.         [ Links ]

6. Alles MS, De Roos NM, Bakx JC, De Lisdonk EV, Zock Pl, Hautvast JG. Consumption of fructooligosaccharides does not favorably affect blood glucose and serum lipid concentrations in patients with type 2 diabetes. Am J Clin Nutr. 1999;69:64-9.         [ Links ]

7. Moore N, Chao C, Yang LP, Storm H, Oliva-emker M, Saavedra JM. Effects of fructo-oligosaccharide-supplemented infant cereal: a double-blind, randomized Trial. Br J Nutr. 2003;90(3):581-7        [ Links ]

8. Maslowski KM, Vieira AT, Ng A, Kranich J, Sierro F, Yu D, Schilter HC, Rolph MS, Mackay F, Artis D, Xavier RJ, Teixeira MM, Mackay CR. Regulation of inûammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature. 2009;461:1282-6.         [ Links ]

9. Sleeth ML, Thompson EL, Ford HE, Zac-Varghese SE, Frost G. Free fatty acid receptor 2 and nutrient sensing: a proposed role for ûbre, fermentable carbohydrates and short-chain fatty acids in appetite regulation. Nutr Res Rev. 2010;23:135-45.         [ Links ]

10. Meijer K, de Vos P, Priebe MG. Butyrate and other short-chain fatty acids as modulators of immunity: what relevance for health? Curr Opin Clin Nutr Metab Care. 2010;13:715-21.         [ Links ]

11. Conterno L, Fava F, Viola R, Tuohy KM. Obesity and the gut microbiota: does up-regulating colonic fermentation protect against obesity and metabolic disease? Genes Nutr. 2011;6:241-60.         [ Links ]

12. Slavin JL. Dietary fiber and body weight. Nutrition. 2005;21:411-8.         [ Links ]

13. Ruppin H, Bar-Meir S, Soergel KH, Wood CM, Schmitt MG. Absorption of short chain fatty acids by the colon. Gastroenterology. 1980;78:1500-7.         [ Links ]

14. Hidaka H, Eida T, Tarizawa T, Tokunaga T, Tashiro Y. Effects of fructo-oligosaccharides on intestinal flora and human health. Bifidobacteria Microflora J. 1986;5:37-50.         [ Links ]

15. Hosoya N, Dhorranintra B, Hidaka H. Utilization of U14-C fructooligosaccharides in man as energy resources. J Clin Biochem Nutr. 1988;5:67-74.         [ Links ]

16. Bornet, FRJ. Undigestible sugars in food products. Am J Clin Nutr. 1994;59:763S-9S.         [ Links ]

17. Alles MS, Hautvasti JGAJ, Nagengast FM, Hartemink R, Van Laere KMJ, Jansen JBMJ. Fate of fructo-oligosaccharides in the human intestine. Br J Nutr. 1996;76: 211-21.         [ Links ]

18. Bergman EN. Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol Rev. 1990;70:567-90.         [ Links ]

19. Boillot J, Alamowitch C, Berger A-M, Luo J, Bruzzo F, Bornet FRJ, Slama G. Effects of dietary propionate on hepatic glucose production, whole-body glucose utilization, carbohydrate and lipid metabolism in normal rats. Br J Nutr. 1995;73:241-1.         [ Links ]

20. Chen WL, Anderson JW. Short chain fatty acid and cholesterol metabolism of rats fed diets supplemented with oat bran. Fed Proc. 1984;43:969-75.         [ Links ]

21. Randle PJ, Garland PB, Hales CN, Newsholme EA. The glucose fatty-acid cycle: its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. Lancet. 1963;281(7285):785-9.         [ Links ]

22. Oberholzer VG, Levin B, Burgess EA, Young WF. Methylmalonic aciduria. An inborn error of metabolism leading to chronic metabolic acidosis. Arch Dis Child. 1967;42:492-504.         [ Links ]

23. Chan TM, Freedland RA. The effect of propionate on the metabolism of pyruvate and lactate in the perfused rat liver. Biochem J. 1972;127:539-3.         [ Links ]

24. Anderson JW, Bridges SR. Short-chain fatty acid fermentation products of plant fiber affect glucose metabolism of isolated rat hepatocytes. Proc Soc Exp Biol Med. 1984;177:372-6.         [ Links ]

25. Blair JG, Cook DE, Lardy HA. Interaction of propionate and lactate in the perfused rat liver. Effects of glucagon and oleate. J Biol Chem. 1973;248:3608-l4.         [ Links ]

26. Yamashita K, Kawai K, Itakura M. Effects of fructo-oligosaccharides on blood glucose and serum lipids in diabetic subjects. Nutr Res. 1984;4:961-6.         [ Links ]

27. Luo J, Rizkalla SW, Alamowitch C, Boussairi A, Blayo A, Barry JL, Laffitte A, Guyon F, Bornet FR, Slama G. Chronic consumption of short-chain fructooligosaccharides by healthy subjects decreased basal hepatic glucose production but had no effect on insulin-stimulated glucose metabolism. Am J Clin Nutr. 1996;63:939-45.         [ Links ]

28. Venter CS, Vorster HH, Cummings, JH. Effects of dietary propionate on carbohydrate and lipid metabolism in healthy volunteers. Am J Gastroenterol. 1990;85:549-53.         [ Links ]

29. Todesco T, Rao AV, Bosello O, Jenkins DJ. Propionate lowers blood glucose and alters lipid metabolism in healthy subjects. Am J Clin Nutr. 1991;54:860-5.         [ Links ]

30. Parnell JA, Reimer RA. Weight loss during oligofructose supplementation is associated with decreased ghrelin and increased peptide YY in overweight and obese adults. Am J Clin Nutr. 2009;89(6):1751-9.         [ Links ]

31. Kim H, Stote KS, Behall KM, Spears K, Vinyard B, Conway JM. Glucose and insulin responses to whole grain breakfasts varying in soluble fiber, beta-glucan: a dose response study in obese women with increased risk for insulin resistance. Eur J Nutr. 2009;48(3):170-5.         [ Links ]

32. De Mello VD, Laaksonen DE. Dietary fibers: current trends and health benefits in the metabolic syndrome and type 2 diabetes. Arq Bras Endocrinol Metab. 2009;53(5):509-18.         [ Links ]

33. Wolever TM, Brighenti F, Royall D, Jenkins AL, Jenkins DJA. Effect of rectal infusion of short chain fatty acids in human subjects. Am J Gastroenterol. 1989;84:1027-33.         [ Links ]

34. Crouse JR, Gerson CD, DeCarli LM, Lieber CS. Role of acetate in the reduction of plasma free fatty acids produced by ethanol in man. J Lipid Res. 1968;9(4):509-12.         [ Links ]

35. Wolever TM, Spadafora P, Eshuis H. Interaction between colonic acetate and propionate in humans. Am J Clin Nutr. 1991;53(3):681-7.         [ Links ]

36. Cummings JH. Short chain fatty acids in the human colon. Gut. 1981;22(9):763-79.         [ Links ]

37. Jenkins DJ, Ghafari H, Wolever TM, Taylor RH, Jenkins AL, Barker HM, Fielden H, Bowling AC. Relationship between rate of digestion of foods and post-prandial glycaemia. Diabetologia. 1982;22(6):450-5.         [ Links ]

38. Jenkins DJ, Wolever TM, Jenkins AL, Thorne MJ, Lee R, Kalmusky J, Reichert R, Wong GS. The glycaemic index of foods tested in diabetic patients: a new basis for carbohydrate exchange favouring the use of legumes. Diabetologia. 1983;24(4):257-64.         [ Links ]

39. Burke BJ, Hartog M, Heaton KW, Hooper S. Assessment of the metabolic effects of dietary carbohydrate and fibre by measuring urinary excretion of C-peptide. Hum Nutr Clin Nutr. 1982;36(5):373-80.         [ Links ]

40. Anderson JW, Ward K. Long-term effects of high-carbohydrate, high-fiber diets on glucose and lipid metabolism: a preliminary report on patients with diabetes. Diabetes Care. 1978;1(2):77-82.         [ Links ]

41. Kinmonth AL, Angus RM, Jenkins PA, Smith MA, Baum JD. Whole foods and increased dietary fibre improve blood glucose control in diabetic children. Arch Dis Child. 1982;57(3):187-94.         [ Links ]

42. Giacco R, Clemente G, Luongo D, Lasorella G, Fiume I, Brouns F, Bornet F, Patti L, Cipriano P, Rivellese AA, Riccardi G. Effects of short-chain fructo-oligosaccharides on glucose and lipid metabolism in mild hypercholesterolaemic individuals. Clin Nutr. 2004;23(3):331-40.         [ Links ]

43. Dominguez-Vergara AM, Vázquez-Moreno L, Montfort GR. Role of prebiotic oligosaccharides in prevention of gastrointestinal infections: a review. Arch Latinoam Nutr. 2009;59(4):358-68.         [ Links ]

 

 

Correspondence:
Sergio Botelho Guimarães
Rua Professor Costa Mendes, 1608/3º andar, Bloco Didático
60430-140 Fortaleza - CE Brasil
Tel.: (55 85)3366-8083
Fax: (55 85)3366-8064
sergiobotelho@terra.com.br

Received: October 10, 2011
Review: December 12, 2011
Accepted: January 11, 2012
Conflict of interest: none
Financial source: none