Abstract
Diets low in fermentable oligo-, di-, and monosaccharides and polyols (FODMAPs) can help reduce symptoms in 50 to 80% of patients suffering from irritable bowel syndrome. Patients are, therefore, often advised to avoid products contributing to FODMAP intake, such as cereal grain products. However, these products are nutritious staple foods and avoiding their consumption may result in nutritional deficiencies. The development of low-FODMAP, high-fiber cereal grain products is therefore desirable. This pilot-scale study shows that Kluyveromyces marxianus CBS6014 (K. marxianus) results in more fructan hydrolysis and a significantly lower final fructan level in white and whole-grain toast bread as well as in rye sourdough bread compared to a commercial Saccharomyces cerevisiae baking strain. Moreover, combined fructan and fructose levels in white and whole-grain bread prepared with K. marxianus remained well below the threshold concentration for low-FODMAP products. In addition to reducing fructan levels, K. marxianus in rye sourdough bread also positively impacted bread height. Whereas further follow-up studies are needed to assess the potential of K. marxianus for bread production fully, our study suggests that this yeast species may open exciting novel routes for the production of low-FODMAP, high-fiber products.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
All data generated or analyzed during this study are included in this published article and its supplementary information files. Raw data can be made available on request.
References
Aguilera-Lizarraga, J., Florens, M. V., Viola, M. F., Jain, P., Decraecker, L., Appeltans, I., et al. (2021). Local immune response to food antigens drives meal-induced abdominal pain. Nature, 590, 151–156. https://doi.org/10.1038/s41586-020-03118-2
Andersson, A. A. M., Andersson, R., Piironen, V., Lampi, A. M., Nyström, L., Boros, D., et al. (2013). Contents of dietary fibre components and their relation to associated bioactive components in whole grain wheat samples from the HEALTHGRAIN diversity screen. Food Chemistry, 136(3–4), 1243–1248. https://doi.org/10.1016/j.foodchem.2012.09.074
Andersson, R., Fransson, G., Tietjen, M., & Åman, P. (2009). Content and molecular-weight distribution of dietary fiber components in whole-grain rye flour and bread. Journal of Agricultural and Food Chemistry, 57(5), 2004–2008. https://doi.org/10.1021/jf801280f
Arica, M. Y., Alaeddinoǧlu, N. G., & Hasirci, V. (1998). Immobilization of glucoamylase onto activated pHEMA/EGDMA microspheres: Properties and application to a packed-bed reactor. Enzyme and Microbial Technology, 22(3), 152–157. https://doi.org/10.1016/S0141-0229(97)00139-7
Aslankoohi, E., Herrera-Malaver, B., Rezaei, M. N., Steensels, J., Courtin, C. M., & Verstrepen, K. J. (2016). Non-conventional yeast strains increase the aroma complexity of bread. PLoS One, 11(10), 1–18. https://doi.org/10.1371/journal.pone.0165126
Birch, A. N., Petersen, M. A., Arneborg, N., & Hansen, Å. S. (2013). Influence of commercial baker’s yeasts on bread aroma profiles. Food Research International, 52(1), 160–166. https://doi.org/10.1016/j.foodres.2013.03.011
Cho, I. H., & Peterson, D. G. (2010). Chemistry of bread aroma: A review. Food Science and Biotechnology, 19(3), 575–582. https://doi.org/10.1007/s10068-010-0081-3
Davidson, M. H., & Maki, K. C. (1999). Effects of dietary inulin on serum lipids. The Journal of Nutrition, 129(7), 1474S-1477S. https://doi.org/10.1093/jn/129.7.1474s
Ford, A. C., & Vandvik, P. O. (2012). Irritable bowel syndrome. BMJ Clinical Evidence, 345, 1–38.
Fraberger, V., Call, L. M., Domig, K. J., & D’Amico, S. (2018). Applicability of yeast fermentation to reduce fructans and other FODMAPs. Nutrients, 10(9). https://doi.org/10.3390/nu10091247
Fretzdorff, B., & Welge, N. (2003). Fructan- und raffinosegehalte im vollkorn einiger getreidearten und pseudo-cerealien. Getreide, Mehl und Brot, 57, 3–8. https://www.tib.eu/en/search/id/BLSE%3ARN126791392/Fructan-und-Raffinosegehalte-im-Vollkorn-einiger/
Gélinas, P., Mckinnon, C., & Gagnon, F. (2016). Fructans, water-soluble fibre and fermentable sugars in bread and pasta made with ancient and modern wheat. International Journal of Food Science and Technology, 51(3), 555–564. https://doi.org/10.1111/ijfs.13022
Gethins, L., Guneser, O., Demirkol, A., Rea, M. C., Stanton, C., Ross, P. R., et al. (2015). Influence of carbon and nitrogen source on production of volatile fragrance and flavour metabolites by the yeast Kluyveromyces marxianus. Yeast, 32, 67–76. https://doi.org/10.1002/yea
Gibson, P. R. (2017). The evidence base for efficacy of the low FODMAP diet in irritable bowel syndrome: is it ready for prime time as a first-line therapy? Journal of Gastroenterology and Hepatology, 32, 32–35. https://doi.org/10.1111/jgh.13693
Gibson, P. R., Newnham, E., Barrett, J. S., Shepherd, S. J., & Muir, J. G. (2007). Review article: Fructose malabsorption and the bigger picture. Alimentary Pharmacology and Therapeutics, 25(4), 349–363. https://doi.org/10.1111/j.1365-2036.2006.03186.x
Gibson, P. R., & Shepherd, S. J. (2010). Evidence-based dietary management of functional gastrointestinal symptoms: The FODMAP approach. Journal of Gastroenterology and Hepatology (Australia), 25(2), 252–258. https://doi.org/10.1111/j.1440-1746.2009.06149.x
Goldstein, R., Braverman, D., & Stankiewicz, H. (2000). Carbohydrate malabsorption and the effect of dietary restriction on symptoms of irritable bowel syndrome and functional bowel complaints. The Israel Medical Association Journal: IMAJ, 2(8), 583-587.
Güneşer, O., Karagül-Yüceer, Y., Wilkowska, A., & Kregiel, D. (2016). Volatile metabolites produced from agro-industrial wastes by Na-alginate entrapped Kluyveromyces marxianus. Brazilian Journal of Microbiology, 47(4), 965–972. https://doi.org/10.1016/j.bjm.2016.07.018
Hadjivasilis, A., Tsioutis, C., Michalinos, A., Ntourakis, D., Christodoulou, D. K., & Agouridis, A. P. (2019). New insights into irritable bowel syndrome: from pathophysiology to treatment. Annals of Gastroenterology, 32(6), 554–564. https://doi.org/10.20524/aog.2019.0428
Halmos, E. P., Power, V. A., Shepherd, S. J., Gibson, P. R., & Muir, J. G. (2014). A diet low in FODMAPs reduces symptoms of irritable bowel syndrome. Gastroenterology, 146(1), 67-75.e5. https://doi.org/10.1053/j.gastro.2013.09.046
Haskå, L., Nyman, M., & Andersson, R. (2008). Distribution and characterisation of fructan in wheat milling fractions. Journal of Cereal Science, 48(3), 768–774. https://doi.org/10.1016/j.jcs.2008.05.002
Hungin, A. P. S., Whorwell, P. J., Tack, J., & Mearin, F. (2003). The prevalence, patterns and impact of irritable bowel syndrome: An international survey of 40,000 subjects. Alimentary Pharmacology and Therapeutics, 17(5), 643–650. https://doi.org/10.1046/j.1365-2036.2003.01456.x
Huynh, B. L., Palmer, L., Mather, D. E., Wallwork, H., Graham, R. D., Welch, R. M., & Stangoulis, J. C. R. (2008). Genotypic variation in wheat grain fructan content revealed by a simplified HPLC method. Journal of Cereal Science, 48(2), 369–378. https://doi.org/10.1016/j.jcs.2007.10.004
Janssen, F., Wouters, A. G. B., Pauly, A., & Delcour, J. A. (2018). Relating the composition and air/water interfacial properties of wheat, rye, barley, and oat dough liquor. Food Chemistry, 264, 126–134. https://doi.org/10.1016/j.foodchem.2018.05.016
Karppinen, S., Myllymäki, O., Forssell, P., & Poutanen, K. (2003). Fructan content of rye and rye products. Cereal Chemistry, 80(2), 168–171. https://doi.org/10.1094/CCHEM.2003.80.2.168
Knez, M., Abbott, C., & Stangoulis, J. C. R. (2014). Changes in the content of fructans and arabinoxylans during baking processes of leavened and unleavened breads. European Food Research and Technology, 239(5), 803–811. https://doi.org/10.1007/s00217-014-2273-1
Knudsen, B. K. E., & Hessov, I. (1995). Recovery of inulin from Jerusalem artichoke (Helianthus tuberosus L.) in the small intestine of man. British Journal of Nutrition, 74(1), 101–113. https://doi.org/10.1079/bjn19950110
Laatikainen, R., Koskenpato, J., Hongisto, S. M., Loponen, J., Poussa, T., Hillilä, M., & Korpela, R. (2016). Randomised clinical trial: low-FODMAP rye bread vs regular rye bread to relieve the symptoms of irritable bowel syndrome. Alimentary Pharmacology and Therapeutics, 44(5), 460–470. https://doi.org/10.1111/apt.13726
Ladas, S. D., Grammenos, I., Tassios, P. S., & Raptis, S. A. (2000). Coincidental malabsorption of lactose, fructose, and sorbitol ingested at low doses is not common in normal adults. Digestive Diseases and Sciences, 45(12), 2357–2362. https://doi.org/10.1023/A:1005634824020
Laurent, J., Timmermans, E., Struyf, N., Verstrepen, K. J., & Courtin, C. M. (2020). Variability in yeast invertase activity determines the extent of fructan hydrolysis during wheat dough fermentation and final FODMAP levels in bread. International Journal of Food Microbiology, 326, 108648. https://doi.org/10.1016/j.ijfoodmicro.2020.108648
Lewis, D. H. (1993). Nomenclature and diagrammatic representation of oligomeric fructans—a paper for discussion. New Phytologist, 124(4), 583–594. https://doi.org/10.1111/j.1469-8137.1993.tb03848.x
Lovell, R. M., & Ford, A. C. (2012). Global prevalence of and risk factors for irritable bowel syndrome: A meta-analysis. Clinical Gastroenterology and Hepatology, 10(7), 712-721.e4. https://doi.org/10.1016/j.cgh.2012.02.029
Makhoul, S., Romano, A., Capozzi, V., Spano, G., Aprea, E., Cappellin, L., et al. (2015). Volatile compound production during the bread-making process: Effect of flour, yeast and their interaction. Food and Bioprocess Technology, 8(9), 1925–1937. https://doi.org/10.1007/s11947-015-1549-1
Marsh, A., Eslick, E. M., & Eslick, G. D. (2016). Does a diet low in FODMAPs reduce symptoms associated with functional gastrointestinal disorders ? A comprehensive systematic review and meta - analysis. European Journal of Nutrition, 55(3), 897–906. https://doi.org/10.1007/s00394-015-0922-1
Maxion-Bergemann, S., Thielecke, F., Abel, F., & Bergemann, R. (2006). Costs of irritable bowel syndrome in the UK and US. PharmacoEconomics, 24(1), 21–37. https://doi.org/10.2165/00019053-200624010-00002
Menezes, L. A. A., Molognoni, L., de Sá Ploêncio, L. A., Costa, F. B. M., Daguer, H., & De Dea Lindner, J. (2019). Use of sourdough fermentation to reducing FODMAPs in breads. European Food Research and Technology, 245(6), 1183–1195. https://doi.org/10.1007/s00217-019-03239-7
Muir, J. G., Varney, J. E., Ajamian, M., & Gibson, P. R. (2019). Gluten-free and low-FODMAP sourdoughs for patients with coeliac disease and irritable bowel syndrome: a clinical perspective. International Journal of Food Microbiology, 290, 237–246. https://doi.org/10.1016/j.ijfoodmicro.2018.10.016
Murray, K., Wilkinson-Smith, V., Hoad, C., Costigan, C., Cox, E., Lam, C., et al. (2014). Differential effects of FODMAPs (Fermentable Oligo-, Di-, Mono-Saccharides and Polyols) on small and large intestinal contents in healthy subjects shown by MRI. American Journal of Gastroenterology, 109(1), 110–119. https://doi.org/10.1038/ajg.2013.386
Norouzian, D., Akbarzadeh, A., Scharer, J. M., & Moo Young, M. (2006). Fungal glucoamylases. Biotechnology Advances, 24(1), 80–85. https://doi.org/10.1016/j.biotechadv.2005.06.003
Nyyssölä, A., Ellilä, S., Nordlund, E., & Poutanen, K. (2020). Reduction of FODMAP content by bioprocessing. Trends in Food Science and Technology, 99, 257–272. https://doi.org/10.1016/j.tifs.2020.03.004
Ong, D. K., Mitchell, S. B., Barrett, J. S., Shepherd, S. J., Irving, P. M., Biesiekierski, J. R., et al. (2010). Manipulation of dietary short chain carbohydrates alters the pattern of gas production and genesis of symptoms in irritable bowel syndrome. Journal of Gastroenterology and Hepatology (Australia), 25(8), 1366–1373. https://doi.org/10.1111/j.1440-1746.2010.06370.x
Palsson, O. S., Whitehead, W., Törnblom, H., Sperber, A. D., & Simren, M. (2020). Prevalence of Rome IV functional bowel disorders among adults in the United States, Canada, and the United Kingdom. Gastroenterology, 158(5), 1262-1273.e3. https://doi.org/10.1053/j.gastro.2019.12.021
Pedersen, N., Vegh, Z., Burisch, J., Jensen, L., Ankersen, D. V., Felding, M., et al. (2014). Ehealth monitoring in irritable bowel syndrome patients treated with low fermentable oligo-, di-, mono-saccharides and polyols diet. World Journal of Gastroenterology, 20(21), 6680–6684. https://doi.org/10.3748/wjg.v20.i21.6680
Pico, J., Bernal, J., & Gómez, M. (2015). Wheat bread aroma compounds in crumb and crust: A review. Food Research International, 75, 200–215. https://doi.org/10.1016/j.foodres.2015.05.051
Ravich, W.J., & Bayless, T. M. (1983). Carbohydrate absorption and malabsorption. Clinics in Gastroenterol, 12(2), 335−356.
Rezaei, M. N., Dornez, E., Jacobs, P., Parsi, A., Verstrepen, K. J., & Courtin, C. M. (2014). Harvesting yeast (Saccharomyces cerevisiae) at different physiological phases significantly affects its functionality in bread dough fermentation. Food Microbiology, 39, 108–115. https://doi.org/10.1016/j.fm.2013.11.013
Schmidt, M., & Sciurba, E. (2020). Determination of FODMAP contents of common wheat and rye breads and the effects of processing on the final contents. European Food Research and Technology, 247(2), 395–410. https://doi.org/10.1007/s00217-020-03633-6
Shepherd, S. J., & Gibson, P. R. (2006). Fructose malabsorption and symptoms of irritable bowel syndrome: Guidelines for effective dietary management. Journal of the American Dietetic Association, 106(10), 1631–1639. https://doi.org/10.1016/j.jada.2006.07.010
Shepherd, S. J., Lomer, M. C. E., & Gibson, P. R. (2013). Short-chain carbohydrates and functional gastrointestinal disorders. American Journal of Gastroenterology, 108(5), 707–717. https://doi.org/10.1038/ajg.2013.96
Shepherd, S. J., Parker, F. C., Muir, J. G., & Gibson, P. R. (2008). Dietary triggers of abdominal symptoms in patients with irritable bowel syndrome: Randomized placebo-controlled evidence. Clinical Gastroenterology and Hepatology, 6(7), 765–771. https://doi.org/10.1016/j.cgh.2008.02.058
Staudacher, H. M., Whelan, K., Irving, P. M., & Lomer, M. C. E. (2011). Comparison of symptom response following advice for a diet low in fermentable carbohydrates (FODMAPs) versus standard dietary advice in patients with irritable bowel syndrome. Journal of Human Nutrition and Dietetics, 24(5), 487–495. https://doi.org/10.1111/j.1365-277X.2011.01162.x
Struyf, N., Laurent, J., Lefevere, B., Verspreet, J., Verstrepen, K. J., & Courtin, C. M. (2017a). Establishing the relative importance of damaged starch and fructan as sources of fermentable sugars in wheat flour and whole meal bread dough fermentations. Food Chemistry, 218, 89–98. https://doi.org/10.1016/j.foodchem.2016.09.004
Struyf, N., Laurent, J., Verspreet, J., Verstrepen, K. J., & Courtin, C. M. (2017b). Saccharomyces cerevisiae and Kluyveromyces marxianus cocultures allow reduction of fermentable oligo-, di-, and monosaccharides and polyols levels in whole wheat bread. Journal of Agricultural and Food Chemistry, 65(39), 8704–8713. https://doi.org/10.1021/acs.jafc.7b02793
Struyf, N., Vandewiele, H., Herrera-Malaver, B., Verspreet, J., Verstrepen, K. J., & Courtin, C. M. (2018). Kluyveromyces marxianus yeast enables the production of low FODMAP whole wheat breads. Food Microbiology, 76, 135–145. https://doi.org/10.1016/j.fm.2018.04.014
Struyf, N., Verspreet, J., & Courtin, C. M. (2016). The effect of amylolytic activity and substrate availability on sugar release in non-yeasted dough. Journal of Cereal Science, 69, 111–118. https://doi.org/10.1016/j.jcs.2016.02.016
Struyf, N., Verspreet, J., Verstrepen, K. J., & Courtin, C. M. (2017c). Investigating the impact of α-amylase, α-glucosidase and glucoamylase action on yeast-mediated bread dough fermentation and bread sugar levels. Journal of Cereal Science, 75, 35–44. https://doi.org/10.1016/j.jcs.2017.03.013
Truswell, A. S., Seach, J. M., & Thorburn, A. W. (1988). Incomplete absorption of pure fructose in healthy subjects and the facilitating effect of glucose. The American Journal of Cinical Nutrition, 48(6), 1424-1430. https://doi.org/10.1093/ajcn/48.6.1424
Tuck, C. J., Muir, J. G., Barrett, J. S., & Gibson, P. R. (2014). Fermentable oligosaccharides, disaccharides, monosaccharides and polyols: Role in irritable bowel syndrome. Expert Review of Gastroenterology and Hepatology, 8(7), 819–834. https://doi.org/10.1586/17474124.2014.917956
Tuck, C. J., Ross, L. A., Gibson, P. R., Barrett, J. S., & Muir, J. G. (2016). Adding glucose to food and solutions to enhance fructose absorption is not effective in preventing fructose-induced functional gastrointestinal symptoms: randomised controlled trials in patients with fructose malabsorption. Journal of Human Nutrition and Dietetics, 30(1), 73–82. https://doi.org/10.1111/jhn.12409
Van den Ende, W. (2013). Multifunctional fructans and raffinose family oligosaccharides. Frontiers in Plant Science. https://doi.org/10.3389/fpls.2013.00247
Van den Houte, K., Carbone, F., Pannemans, J., Corsetti, M., Fischler, B., Piessevaux, H., & Tack, J. (2019). Prevalence and impact of self-reported irritable bowel symptoms in the general population. United European Gastroenterology Journal, 7(2), 307–315. https://doi.org/10.1177/2050640618821804
Varney, J., Barrett, J., Scarlata, K., Catsos, P., Gibson, P. R., & Muir, J. G. (2017). FODMAPs: Food composition, defining cutoff values and international application. Journal of Gastroenterology and Hepatology (Australia), 32, 53–61. https://doi.org/10.1111/jgh.13698
Verspreet, J., Hansen, A. H., Harrison, S. J., Vergauwen, R., Van den Ende, W., & Courtin, C. M. (2017). Building a fructan LC–MS2 library and its application to reveal the fine structure of cereal grain fructans. Carbohydrate Polymers, 174, 343–351. https://doi.org/10.1016/j.carbpol.2017.06.063
Verspreet, J., Hemdane, S., Dornez, E., Cuyvers, S., Delcour, J. A., & Courtin, C. M. (2013). Maximizing the concentrations of wheat grain fructans in bread by exploring strategies to prevent their yeast (Saccharomyces cerevisiae)-mediated degradation. Journal of Agricultural and Food Chemistry, 61(6), 1397–1404. https://doi.org/10.1021/jf3050846
Verspreet, J., Pollet, A., Cuyvers, S., Vergauwen, R., Van Den Ende, W., Delcour, J. A., & Courtin, C. M. (2012). A simple and accurate method for determining wheat grain fructan content and average degree of polymerization. Journal of Agricultural and Food Chemistry, 60(9), 2102–2107. https://doi.org/10.1021/jf204774n
Verstrepen, K. J., Iserentant, D., Malcorps, P., Derdelinckx, G., Van Dijck, P., Winderickx, J., et al. (2004). Glucose and sucrose: Hazardous fast-food for industrial yeast? Trends in Biotechnology, 22(10), 531–537. https://doi.org/10.1016/j.tibtech.2004.08.001
Whelan, K., Abrahmsohn, O., David, G. J. P., Staudacher, H., Irving, P., Lomer, M. C. E., & Ellis, P. R. (2011). Fructan content of commonly consumed wheat, rye and gluten-free breads. International Journal of Food Sciences and Nutrition, 62(5), 498–503. https://doi.org/10.3109/09637486.2011.553588
Wilkowska, A., Kregiel, D., Guneser, O., & Yuceer, Y. K. (2015). Growth and by-product profiles of Kluyveromyces marxianus cells immobilized in foamed alginate. Yeast, 32, 217–225. https://doi.org/10.1002/yea
Ziegler, J. U., Steiner, D., Longin, C. F. H., Würschum, T., Schweiggert, R. M., & Carle, R. (2016). Wheat and the irritable bowel syndrome—FODMAP levels of modern and ancient species and their retention during bread making. Journal of Functional Foods, 25, 257–266. https://doi.org/10.1016/j.jff.2016.05.019
Acknowledgements
Jitka Laurent thanks the Fonds Wetenschappelijk Onderzoek-Vlaanderen for the financial support (Grant number 11A1620N).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Laurent, J., Struyf, N., Bautil, A. et al. The Potential of Kluyveromyces marxianus to Produce Low-FODMAP Straight-Dough and Sourdough Bread: a Pilot-Scale Study. Food Bioprocess Technol 14, 1920–1935 (2021). https://doi.org/10.1007/s11947-021-02681-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11947-021-02681-4