Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

Influence of the type of indigestible carbohydrate on plasma and urine short-chain fatty acid profiles in healthy human volunteers

Abstract

Background/Objectives:

Health effects of whole grain foods are becoming more evident. In this study, we analysed the short-chain fatty acid profiles in urine and serum derived from the colonic fermentation process of 13C-barley meals, prepared from barley grown under 13CO2 atmosphere.

Subjects/Methods:

In a crossover study, five volunteers ingested intact barley kernels (high content of non-starch polysaccharides (NSP) and resistant starch (RS)) and barley porridge (high content of NSP only). Using a newly developed stable isotope technology, we monitored 14 and 24 h postprandially 13C-acetate, 13C-propionate and 13C-butyrate in plasma and urine, respectively. The oro-cecal transit time (OCTT) of the meals was measured with the hydrogen breath test.

Results:

The OCTT was 6 h and did not differ between the two test meals. An increase of 13C-acetate was observed already early after ingestion of the meals (<6 h) and was attributed to early fermentation of the test meal. A rise in plasma 13C-propionate in the fermentation phase could only be detected after the porridge and not after the kernel meal. An increase in 13C-butyrate was only found in the fermentation phase and was higher after the barley kernels. Urine 13C-short-chain fatty acids data were consistent with these observations.

Conclusions:

The difference in the profiles of 13C-acetate, 13C-propionate and 13C-butyrate indicates that NSP combined with RS results in an altered fermentation profile than dietary fibre alone.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2

Similar content being viewed by others

References

  • Ahmed R, Segal I, Hassan H (2000). Fermentation of dietary starch in humans. Am J Gastroenterol 95, 1017–1020.

    Article  CAS  PubMed  Google Scholar 

  • Anderson JW, Bridges SR (1984). Short-chain fatty acid fermentation products of plant fiber affect glucose metabolism of isolated rat hepatocytes. Proc Soc Exp Biol Med 177, 372–376.

    Article  CAS  PubMed  Google Scholar 

  • Anderson JW, Hanna TJ, Peng XJ, Kryscio RJ (2000). Whole grain foods and heart disease risk. J Am Coll Nutr 19, 291S–299S.

    Article  CAS  PubMed  Google Scholar 

  • Bird AR, Jackson M, King RA, Davies DA, Usher S, Topping DL (2004). A novel high-amylose barley cultivar (Hordeum vulgare var. Himalaya 292) lowers plasma cholesterol and alters indices of large-bowel fermentation in pigs. Br J Nutr 92, 607–615.

    Article  CAS  PubMed  Google Scholar 

  • Brighenti F, Benini L, Del Rio D, Casiraghi C, Pellegrini N, Scazzina F et al. (2006). Colonic fermentation of indigestible carbohydrates contributes to the second-meal effect. Am J Clin Nutr 83, 817–822.

    Article  CAS  PubMed  Google Scholar 

  • Brouns F, Kettlitz B, Arrigoni E (2002). Resistant starch and ‘the butyrate revolution’. Trends Food Sci Technol 13, 251–261.

    Article  CAS  Google Scholar 

  • Brown AJ, Goldsworthy SM, Barnes AA, Eilert MM, Tcheang L, Daniels D et al. (2003). The orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J Biol Chem 278, 11312–11319.

    Article  CAS  PubMed  Google Scholar 

  • Casterline JL, Oles CJ, Ku Y (1997). In vitro fermentation of various food fiber fractions. J Agric Food Chem 45, 2463–2467.

    Article  CAS  Google Scholar 

  • De Schrijver R, Vanhoof K, Vande Ginste J (1999). Effect of enzyme resistant starch on large bowel fermentation in rats and pigs. Nutr Res 19, 927–936.

    Article  CAS  Google Scholar 

  • Falony G, Vlachou A, Verbrugghe K, De Vuyst L (2006). Cross-feeding between Bifidobacterium longum BB536 and acetate-converting, butyrate-producing colon bacteria during growth on oligofructose. Appl Environ Microbiol 72, 7835–7841.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferchaud-Roucher V, Albert C, Champ M, Krempf M (2006). Solid-phase microextraction method for carbon isotopic analysis of volatile carboxylic acids in human plasma by gas chromatography/combustion/isotope ratio mass spectrometry. Rapid Commun Mass Spectrom 20, 3573–3578.

    Article  CAS  PubMed  Google Scholar 

  • Ferchaud-Roucher V, Pouteau E, Piloquet H, Zair Y, Krempf M (2005). Colonic fermentation from lactulose inhibits lipolysis in overweight subjects. Am J Physiol Endocrinol Metab 289, E716–E720.

    Article  CAS  PubMed  Google Scholar 

  • Fushimi T, Suruga K, Oshima Y, Fukiharu M, Tsukamoto Y, Goda T (2006). Dietary acetic acid reduces serum cholesterol and triacylglycerols in rats fed a cholesterol-rich diet. Br J Nutr 95, 916–924.

    Article  CAS  PubMed  Google Scholar 

  • Geypens B, Bennink R, Peeters M, Evenepoel P, Mortelmans L, Maes B et al. (1999). Validation of the lactose-[13C]ureide breath test for determination of orocecal transit time by scintigraphy. J Nucl Med 40, 1451–1455.

    CAS  PubMed  Google Scholar 

  • Ghoos YF, Maes BD, Geypens BJ, Mys G, Hiele MI, Rutgeerts PJ et al. (1993). Measurement of gastric-emptying rate of solids by means of a carbon-labeled octanoic-acid breath test. Gastroenterology 104, 1640–1647.

    Article  CAS  PubMed  Google Scholar 

  • Gimeno RE, Klaman LD (2005). Adipose tissue as an active endocrine organ: recent advances. Curr Opin Pharmacol 5, 122–128.

    Article  CAS  PubMed  Google Scholar 

  • Haycock GB, Schwartz GJ, Wisotsky DH (1978). Geometric method for measuring body-surface area—height-weight formula validated in infants, children, and adults. J Pediatr 93, 62–66.

    Article  CAS  PubMed  Google Scholar 

  • Henningsson AM, Bjorck IME, Nyman EM (2002). Combinations of indigestible carbohydrates affect short-chain fatty acid formation in the hindgut of rats. J Nutr 132, 3098–3104.

    Article  CAS  PubMed  Google Scholar 

  • Higgins J, Brown M, Storlien L (2006). Consumption of resistant starch decreases postprandial lipogenesis in white adipose tissue of the rat. Nutr J 5, 25.

    Article  PubMed  PubMed Central  Google Scholar 

  • Higgins J, Higbee D, Donahoo W, Brown I, Bell M, Bessesen D (2004). Resistant starch consumption promotes lipid oxidation. Nutr Metab 1, 8.

    Article  Google Scholar 

  • Hughes SA, Shewry PR, Gibson GR, McCleary BV, Rastall RA (2008). In vitro fermentation of oat and barley derived beta-glucans by human faecal microbiota. Fems Microbiol Ecol 64, 482–493.

    Article  CAS  PubMed  Google Scholar 

  • Ito H, Yuto S, Motoi H, Yagishita T, Takeya K, Sugiyama K et al. (2006). Partial replacement of waxy cornstarch by recrystallized amylose retards the development of insulin resistance in rats. Biosci Biotechnol Biochem 70, 2429–2436.

    Article  CAS  PubMed  Google Scholar 

  • Kabir M, Rizkalla SW, Champ M, Luo J, Boillot J, Bruzzo F et al. (1998). Dietary amylose-amylopectin starch content affects glucose and lipid metabolism in adipocytes of normal and diabetic rats. J Nutr 128, 35–42.

    Article  CAS  PubMed  Google Scholar 

  • Koh-Banerjee P, Rimm EB (2003). Whole grain consumption and weight gain: a review of the epidemiological evidence, potential mechanisms and opportunities for future research. Proc Nutr Soc 62, 25–29.

    Article  CAS  PubMed  Google Scholar 

  • Kok N, Roberfroid M, Robert A, Delzenne N (1996). Involvement of lipogenesis in the lower VLDL secretion induced by oligofructose in rats. Br J Nutr 76, 881–890.

    Article  CAS  PubMed  Google Scholar 

  • Livesey G, Wilkinson JA, Roe M, Faulks R, Clark S, Brown JC et al. (1995). Influence of the physical form of barley-grain on the digestion of its starch in the human small-intestine and implications for health. Am J Clin Nutr 61, 75–81.

    Article  CAS  PubMed  Google Scholar 

  • McKeown NM, Meigs JB, Liu SM, Wilson PWF, Jacques PF (2002). Whole-grain intake is favorably associated with metabolic risk factors for type 2 diabetes and cardiovascular disease in the Framingham Offspring Study. Am J Clin Nutr 76, 390–398.

    Article  CAS  PubMed  Google Scholar 

  • Morrison DJ, Cooper K, Waldron S, Slater C, Weaver LT, Preston T (2004). A streamlined approach to the analysis of volatile fatty acids and its application to the measurement of whole-body flux. Rapid Commun Mass Spectrom 18, 2593–2600.

    Article  CAS  PubMed  Google Scholar 

  • Morrison DJ, Mackay WG, Edwards CA, Preston T, Dodson B, Weaver LT (2006). Butyrate production from oligofructose fermentation by the human faecal flora: what is the contribution of extracellular acetate and lactate? Br J Nutr 96, 570–577.

    CAS  PubMed  Google Scholar 

  • Nilsson A, Granfeldt Y, Ostman E, Preston T, Bjorck I (2006). Effects of GI and content of indigestible carbohydrates of cereal-based evening meals on glucose tolerance at a subsequent standardised breakfast. Eur J Clin Nutr 60, 1092–1099.

    Article  CAS  PubMed  Google Scholar 

  • Nishina PM, Freedland RA (1990). Effects of propionate on lipid biosynthesis in isolated rat hepatocytes. J Nutr 120, 668–673.

    Article  CAS  PubMed  Google Scholar 

  • Pomare EW, Branch WJ, Cummings JH (1985). Carbohydrate fermentation in the human colon and its relation to acetate concentrations in venous blood. J Clin Invest 75, 1448–1454.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pouteau E, Vahedi K, Messing B, Flourie B, Nguyen P, Darmaun D et al. (1998). Production rate of acetate during colonic fermentation of lactulose: a stable-isotope study in humans. Am J Clin Nutr 68, 1276–1283.

    Article  CAS  PubMed  Google Scholar 

  • Pylkas AM, Juneja LR, Slavin JL (2005). Comparison of different fibers for in vitro production of short chain fatty acids by intestinal microflora. J Med Food 8, 113–116.

    Article  CAS  PubMed  Google Scholar 

  • Robertson MD, Bickerton AS, Dennis AL, Vidal H, Frayn KN (2005). Insulin-sensitizing effects of dietary resistant starch and effects on skeletal muscle and adipose tissue metabolism. Am J Clin Nutr 82, 559–567.

    Article  CAS  PubMed  Google Scholar 

  • Robertson MD, Currie JM, Morgan LM, Jewell DP, Frayn KN (2003). Prior short-term consumption of resistant starch enhances postprandial insulin sensitivity in healthy subjects. Diabetologia 46, 659–665.

    Article  CAS  PubMed  Google Scholar 

  • Smiricky-Tjardes MR, Flickinger EA, Grieshop CM, Bauer LL, Murphy MR, Fahey GC (2003). In vitro fermentation characteristics of selected oligosaccharides by swine fecal microflora. J Anim Sci 81, 2505–2514.

    Article  CAS  PubMed  Google Scholar 

  • Tannock GW (1995). Normal Microflora. Chapma & Hall: London.

    Google Scholar 

  • Velazquez M, Davies C, Marett R, Slavin JL, Feirtag JM (2000). Effect of oligosaccharides and fibre substitutes on short-chain fatty acid production by human faecal microflora. Anaerobe 6, 87–92.

    Article  CAS  Google Scholar 

  • Venter CS (1990). Effects of dietary propionate on carbohydrate and lipid metabolism in healthy volunteers. Am J Gastroenterol 85, 549–553.

    CAS  PubMed  Google Scholar 

  • Weaver GA, Krause JA, Miller TL, Wolin MJ (1992). Cornstarch fermentation by the colonic microbial community yields more butyrate than does cabbage fiber fermentation—cornstarch fermentation rates correlate negatively with methanogenesis. Am J Clin Nutr 55, 70–77.

    Article  CAS  PubMed  Google Scholar 

  • Weickert MO, Mohlig M, Schofl C, Arafat AM, Otto B, Viehoff H et al. (2006). Cereal fiber improves whole-body insulin sensitivity in overweight and obese women. Diabetes Care 29, 775–780.

    Article  CAS  PubMed  Google Scholar 

  • Wolever TMS, Brighenti F, Royall D, Jenkins AL, Jenkins DJA (1989). Effect of rectal infusion of short chain fatty acids in human subjects. Am J Gastroenterol 84, 1027–1033.

    CAS  PubMed  Google Scholar 

  • Xiong YM, Miyamoto N, Shibata K, Valasek MA, Motoike T, Kedzierski RM et al. (2004). Short-chain fatty acids stimulate leptin production in adipocytes through the G protein-coupled receptor GPR41. Proc Natl Acad Sci USA 101, 1045–1050.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank D Binnema and P Sanders from TNO, Quality of Life, Groningen, The Netherlands for in vitro starch analysis of the test meals. This work was financially supported by the Commission of the European Communities, and specifically the RTD programme ‘Quality of Life and Management of Living Resources’, QLK 1-2001-00431 ‘Stable isotope applications to monitor starch digestion and fermentation for the development of functional foods’ (EUROSTARCH). This work does not necessarily reflect its views and in no way anticipates the Commission's future policy in this area. Further financial support was obtained from the Fund for Scientific Research-Flanders (F.W.O.-Vlaanderen, Belgium).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to K Verbeke.

Ethics declarations

Competing interests

The authors declare no conflict of interest.

Additional information

Supplementary Information accompanies the paper on European Journal of Clinical Nutrition website

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Cite this article

Verbeke, K., Ferchaud-Roucher, V., Preston, T. et al. Influence of the type of indigestible carbohydrate on plasma and urine short-chain fatty acid profiles in healthy human volunteers. Eur J Clin Nutr 64, 678–684 (2010). https://doi.org/10.1038/ejcn.2010.92

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ejcn.2010.92

Keywords

This article is cited by

Search

Quick links