Reduction of FODMAP content by bioprocessing

Journal Pre-proof Reduction of FODMAP content by bioprocessing Antti Nyyssölä, Simo Ellilä, Emilia Nordlund, Kaisa Poutanen

PII:

S0924-2244(19)30925-2

DOI:

https://doi.org/10.1016/j.tifs.2020.03.004

Reference:

TIFS 2773

To appear in:

Trends in Food Science & Technology

Received Date: 2 November 2019 Revised Date:

3 March 2020

Accepted Date: 6 March 2020

Please cite this article as: Nyyssölä, A., Ellilä, S., Nordlund, E., Poutanen, K., Reduction of FODMAP content by bioprocessing, Trends in Food Science & Technology (2020), doi: https://doi.org/10.1016/ j.tifs.2020.03.004. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Published by Elsevier Ltd.

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ABSTRACT

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Background Fermentable oligo- di- and mono-saccharides and polyols, abbreviated as FODMAP, are components of several plant-based foods as well as milk. The FODMAPs include fructans and galacto-oligosaccharides, lactose, fructose, and sugar alcohols. Ingestion of FODMAPs may trigger gastrointestinal symptoms in people with functional bowel disorders, such as the irritable bowel syndrome (IBS).

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Scope and approach Studies have shown that a low-FODMAP diet improves symptoms of IBS. However, restricting the intake of FODMAP-rich foods is problematic, since many of them are rich in components important for health, such as dietary fibre, vitamins and minerals. This review describes the possibility of targeted FODMAP removal from foods by bioprocessing. Since the source of majority of FODMAPs are plant-based foods, such as fruits, grains, pulses and vegetables, FODMAP reduction by bioprocessing is also of interest in terms of the transition to more plant-based diets.

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Key findings and conclusions Levels of galacto-oligosaccharides, fructans and lactose can be significantly reduced by enzymatic treatment, fermentation and germination. Enzyme-aided FODMAP reduction is typically specific, whereas during fermentation and germination several enzymes are active, which may influence food characteristics via polymer degradation and metabolite formation. Enzymatic processing and fermentation can usually be implemented in hours, whereas germination is relatively slow process, taking days. Implications of targeted FODMAP reduction in foods by bioprocessing should be considered in particular from nutritional, sensory and tolerance perspectives.

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Reduction of FODMAP content by bioprocessing

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Antti Nyyssölä*, Simo Ellilä, Emilia Nordlund, Kaisa Poutanen

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VTT Technical Research Centre of Finland Ltd., Solutions for Natural Resources and Environment, P.O. Box 1000, FIN-02044 VTT, Finland.

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*

Corresponding author [email protected]

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Introduction

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Fermentable Oligo- Di- and Monosaccharides and Polyols, abbreviated as FODMAP, are components of milk and many plant-based foods. FODMAP include fructans and galactooligosaccharides, lactose, fructose when in excess to glucose, sorbitol, mannitol and xylitol (Fig. 1). Intake of FODMAPs may exacerbate gastrointestinal symptoms in people with functional bowel disorders, such as the irritable bowel syndrome (IBS). The proposed reason for this is that since FODMAP compounds are poorly absorbed in the small intestine, they pass to the large intestine, where gut bacteria rapidly ferment them to short chain fatty acids and gases. FODMAP compounds may also exhibit osmotic effects, drawing water into the large intestine, which leads to diarrhea (Gibson & Shepherd, 2005). Typical foods and raw materials containing FODMAP compounds include legumes, cereals, dairy and fruit (Table 1).

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The low-FODMAP diet, which alleviates symptoms of both adult and child patients with IBS, consists of three phases. First, the FODMAP-rich foods are omitted from the diet, after which they are reintroduced separately to determine which FODMAPS and foods trigger the symptoms. In the third phase the diet is personalized by reintroducing the tolerated foods and FODMAPS, while avoiding symptom causing foods (Chumpitazi et al., 2015; Halmos, Power, Shepherd, Gibson, & Muir, 2014; Hill, Muir, & Gibson, 2017a). However, it seems that in public discussion and practices the two latter phases are often not remembered.

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Varney et al. (2017) have defined low-FODMAP cutoff values for each FODMAP carbohydrate (per serving of food per meal) of the low-FODMAP diet for IBS patients. For grain, legume, nut and seed oligosaccharides (fructan and α-galacto-oligosaccharides), the cutoff value is <0.3 g per serving, whereas for vegetable, fruit and other food oligosaccharides it is <0.2 g per serving. When fructose in excess to glucose is the only FODMAP present (for fruit or vegetables), the cutoff is <0.4 g per serving. When there are other FODMAP present, the value for fructose in excess to glucose is <0.15 g per serving. For sorbitol or mannitol the limit is at <0.2 g per serving, while for total polyols it is <0.4 g per serving. For lactose the suggested cutoff value is <1.0 g per serving.

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The relevance of negatively perceived gastrointestinal effects of FODMAP compounds is increasing along with the need to transition towards more plant-based diets that has been recommended by the Intergovernmental Panel on Climate Change (IPCC) (Schiermeier, 2019). With an attempt to develop plant-based foods suitable for all consumers, solutions to reduce FODMAP content are becoming more important. A dietary therapy based on avoiding FODMAP rich foods, does not seem to be a sustainable solution for large consumer segments. Moreover, avoiding foods with FODMAP compounds can results in low dietary fibre and

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phytochemical intake with negative impact on health (Hill, Muir, & Gibson, 2017b; Muir & Gibson, 2013).

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Since the introduction of the FODMAP concept in 2005 (Gibson & Shepherd, 2005), it has been a topic of increasing scientific and commercial interest. The occurrence of FODMAP compounds and their relevance in gastrointestinal symptoms has been the subject of a number of recent reviews (Barrett, 2017; Hill et al., 2017; Tuck et al., 2018a; Varney et al., 2017). On the other hand, many FODMAP compounds (fructans, α-galacto-oligosaccharides) are a part of dietary fibre, the health protective effects of which are widely recognized (Makki, Deehan, Walter, & Bäckhed, 2018). Dietary fibre is a very diverse and heterogenic group of compounds, and should therefore be specified when studying its physiological effects (Poutanen et al., 2017). The non-digestible α-oligosaccharides in food have already earlier been of scientific and commercial interest due to their prebiotic effects, i.e. “The selective stimulation of growth and/or activity(ies) of one or a limited number of microbial genus(era)/species in the gut microbiota that confer(s) health benefits to the host” (Roberfroid et al., 2010). These compounds were, as part of dietary fibre, considered mainly for their health benefits and their gastrointestinal tolerance has been studied in healthy humans. Daily doses of 5-10 g of inulin have been reported to be well tolerated depending on the DP (degree of polymerization) distribution of the product (Bonnema, Kolberg, Thomas, & Slavin, 2010; Bruhwyler, Carreer, Demanet, & Jacobs, 2009). Even though all FODMAP are not prebiotic or dietary fibre, comparing this data with the FODMAPtolerance data in people with gastrointestinal disorders shows the large variation of tolerance to gastrointestinal fermentation rate in humans.

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Some nonprescription dietary supplements with specific FODMAP hydrolyzing enzymes such as lactase (e.g. Lactaid® or Lactrase®) and α-galactosidase (e.g. Beano® or Bean ReliefTM) are commercially available for managing FODMAP related symptoms. However, these products are relatively expensive and the reaction conditions (pH, incubation time) of the gastrointestinal tract are not necessarily optimal for achieving high enough hydrolysis degrees. An interesting alternative to achieve a low-FODMAP diet is to specifically reduce the FODMAP content in foods, allowing intake of other useful nutrients from these foods. This can be conducted via degradation of the FODMAP compounds in food raw materials and during food processing by exogenous enzymes. A list of FODMAP degrading enzymes is presented in Table 2. Other ways of bioprocessing, such as fermentation and germination, may also reduce FODMAP content in food processing, as reviewed for sourdough by Loponen & Gänzle (2018). The current review presents research and solutions for removal of FODMAP compounds by bioprocessing. The focus is on fructan, α-galacto-oligosaccharide and lactose removal with enzyme-aided solutions and fermentative processes as well as by activation of endogenous enzymes by germination.

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Fructans

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It has been estimated that approximately 15% of flowering plants produce fructan polymers as carbohydrate storage materials. Fructans may also have other functions in plants, such as protection against drought and low temperature. Plant fructans are structurally diverse molecules, which can be divided into several classes depending on the nature of the linkages. Inulin, which is typical for e.g. chicory and Jerusalem artichoke, is a linear polymer with β(1-2)linkages between the fructose molecules (Fig. 1 a). Levans (or phleins) that are formed by linear β(2-6)-linked fructose units are produced by bacteria and some grasses. Mixed levan, which contains both β(1-2) and β(2-6)-links, is present in wheat and barley. Inulin and levan neoseries have a glucose moiety between two polymer chains. Inulin neoseries is found in e.g. onion and asparagus and levan neoseries in oat. Although most fructan molecules have a chain-terminating glucosyl moiety, fructans consisting solely of fructose have also been isolated, for instance from chicory and Jerusalem artichoke (Vijn & Smeekens, 1999).

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For plant fructans the degree of polymerization typically ranges from 2 to 60 monosaccharide units, but can in some cases exceed 200 units (Roberfroid, 1993; Vijn & Smeekens, 1999). Plant fructans with degrees of polymerization of 2 to 20 have been defined as fructooligosaccharides (FOS) by Roberfroid (1993).

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Fructans are common components of many vegetables such as onions (1.1-7.5% dw), Jerusalem artichoke (16-20% ww), leek (3-10% ww), garlic (9-16% ww), and some fruits such as banana (0.3-0.7% ww) (Van Loo, Coussement, De Leenheer, Hoebregs, & Smits, 1995) (Table 1). Wheat and rye are generally consumed in relatively large amounts in countries with temperate climates (including Western countries, Russia, Near and Middle East and the North of China). They are therefore, especially when used as whole-grain, a significant source fructans, although their fructan concentrations range only between 3.6 and 6.6% dw for rye and between 0.7 and 2.9 % dw for wheat (Verspreet, Dornez, Van den Ende, Delcour, & Courtin, 2015).

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Enzymatic removal

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Since humans lack the enzymes hydrolysing fructans to fructose, these polymers cannot be absorbed in the intestine (Gibson, Newnham, Barrett, Shepherd, & Muir, 2006). However, fructan degrading enzymes are common for other organisms such as many plants and microbes (Vijn & Smeekens, 1999).

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Inulinases catalyze the hydrolysis of β(2-1) glycosidic linkages of inulin. Exoinulinases (EC 3.2.1.80) are specific for the terminal linkages of inulin and release fructose, whereas

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endoinulinases (EC 3.2.1.7) target the internal β(2-1) glycosidic linkages, producing FOS such as inulotriose, inulotetraose and inulopentaose as the main products. Invertase (βfructofuranoside fructohydrolase EC 3.2. 1.26) has also been shown to catalyze inulin degradation by an exo-mechanism (Wang & Li, 2013).

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The characterized inulinases typically have pH optima at slightly acidic or neutral pH (pH 4-7.6) and are produced by a wide variety of fungi, yeasts and bacteria (Rawat, Soni, Treichel, & Kango, 2017; Singh & Singh, 2017). Endoinulinases have previously been used for the production of FOSs from chicory inulin for use as low-calorie sweeteners (Roberfroid, 2004). An endoinulinase preparation was previously commercially available under the brand name Fructozyme L (Novozymes) for this purpose.

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There are also a number of other fructan-degrading enzymes identified from various organisms. These include endo-acting levanases (EC 3.2.1.65) catalyzing the random hydrolysis of β(2-6)-linkages of levans containing more than three fructose units (Chaudhary, Gupta, Gupta, & Banerjee, 1996). To our knowledge there have been no attempts to utilize levanasetype-of enzymes in food processing.

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A fructanase (inulinase) enzyme for lowering the fructan level of rye bread has been described in a patent application by Fazer Bakeries (Finland) (Loponen, Mikola, & Sibakov, 2017). For isolating the fructanase producer a sourdough seed starter was generated using grain material with a low content of damaged starch, (e.g. whole, peeled or cut kernels). Milling damages starch granules and starch becomes thereby available as a growth substrate for amylolytic microbes of the sourdough flora. Maltose, which is released by amylases under these conditions becomes the main carbohydrate source for microbes. However, in the absence of damaged starch fructans are utilized instead, which leads to enrichment of microbes capable of hydrolyzing it. Enrichment can be continued by so-called back-slopping, which means inoculation of the next batch of sourdough with a fraction of the previous one (Loponen, 2016).

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The repeated back-slopping process was the source for the bacterial fructanase producer, identified as Lactobacillus crispatus. The fructanase enzyme was produced recombinantly in Pichia pastoris and tested for degradation of different types of fructan substrates on the basis of released fructose. Oligomeric fructans (4 g/L) were degraded nearly quantitatively (97% of hydrolysis). Fructans (4 g/L) with average degrees of polymerizations of 10 and 23 were 76% and 55% hydrolysed, respectively, and with rye meal extract (2 g/L) as the substrate, 81% hydrolysis of the fructan type of compounds was achieved. As pointed out by the inventors, hydrolysis of the fructan polymer also resulted in formation of FOS, which are also FODMAP compounds, and presumably more easily fermented by gut microbes than the polymer. In the case of the oligomers, the shorter inulin substrate and rye extract the decrease in substrate

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concentrations correlated well with the amount of fructose released. The longer inulin substrate was removed by 32% which is considerably less than the release of fructose (55 %) suggesting oligomer generation. The enzyme preparation is now commercially available by the name LOFOTM, and is claimed to decrease the fructan content of grain products by more than 50%. For instance, the patent describes a reduction of 90% for rye bread. In addition to fructan reduction in dough, the fructanase was shown to also degrade fructan from garlic (60% reduction) and Jerusalem artichoke (68% reduction) (Loponen et al., 2017). Examples of reduction of fructan content of foods using enzymes are presented in Table 3. It should be noted that the product of fructan hydrolysis, fructose, is also classified as a FODMAP, when it is present in excess to glucose. It may be possible to remove the excess fructose by fermentation (see below) or further enzymatic steps.

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The use of fructanases for degradation of dough fructans have also been described for other purposes. In a patent application by Novozymes AS, fructans are hydrolyzed to FOS and fructose by Fructozyme L (Novozymes) to achieve increased bread softness (Meier, Ritting, & Drost-Lustenberger, 2011). In another patent application by Mauri Technology Bv, added inulin is hydrolyzed with fructanases and an invertase to simple sugars, to sweeten the bread (Branco & Van Oort, 2018).

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Removal by fermentation

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During baking, endogenous, microbial, or added amylases and other carbohydrate hydrolyzing enzymes break down starch to fermentable sugars such as maltose. Dough can then be leavened by bacterial and/or yeast fermentation of the sugars to carbon dioxide to achieve increased volume and fluffiness. Saccharomyces cerevisiae (baker’s yeast) is the most common biological leavening agent used in present-day bakeries (Catzeddu, 2011; Melim Miguel, Souza Martins-Meyer, da Costa Figueiredo, Paulo Lobo, & Dellamora-Ortiz, 2013). It produces an invertase, which in addition to cleaving sucrose to fructose and glucose has hydrolytic activity towards short-chain fructooligosaccharides (Sainz-Polo et al., 2013; Verspreet et al., 2013). S. cerevisiae invertase is either intracellular or remains mostly cell-wall associated (Esmon, Esmon, Schauer, Taylor, & Schekman, 1987), which may hinder its access to the fructans present in the bulk of the dough. It has nevertheless been reported that between 40 to 80% of wheat fructans can be degraded during baking with S. cerevisiae (Gélinas, McKinnon, & Gagnon, 2016; Knez, Abbott, & Stangoulis, 2014; Nilsson, Öste, & Jägerstad, 1987; Verspreet et al., 2013). However, it has been claimed that in real-life the extents of reduction achieved are usually not high enough for people sensitive to FODMAP compounds (Struyf, Laurent, Verspreet, Verstrepen, & Courtin, 2017). As described above, fructose, which is the degradation product of fructan, is also classified as a FODMAP, when it is present in excess to glucose. Extending the fermentation time can have a major impact on the final FODMAP levels in the bread. It has been shown that prolonging wheat dough

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proofing time from 1 h to over 4 h diminishes the total FODMAP level (fructose included), by 90% (Ziegler et al., 2016). Examples of reduction of fructan contents of foods during bread making are presented in Table 3.

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Kluyveromyces marxianus is a yeast with GRAS (Generally Recognized As Safe) status that produces both secreted and cell-wall attached fructanases, which efficiently catalyze fructan degradation (Rouwenhorst, Hensing, Verbakel, Scheffers, & van Duken, 1990). Using it as a monoculture for leavening is, however, not feasible, since it is not capable of fermenting maltose (Van der Walt & Johannsen, 1970), which is the main fermentable sugar released from damaged starch (Struyf, Van der Maelen, et al., 2017). K. marxianus has therefore been used in co-culture with S. cerevisiae to achieve more extensive fructan degradation as well as high enough carbon dioxide production. A reduction of over 90% in the fructan content was achieved by leavening with the co-culture, whereas only 56% of the fructan was degraded by S. cerevisiae alone. In addition, the volumes of the loafs were not significantly different. However, as the authors of the study noted, K. marxianus acted mainly as a fructanase source in the co-culture instead of as a carbon dioxide producer. Similar results may therefore have been achieved by addition of an exogenous fructanase (Struyf, Laurent, et al., 2017). In addition, co-cultures are more difficult to produce for industrial scale use than monocultures (Struyf et al., 2018).

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Struyf and co-workers also studied the possibility of using a monoculture of K. lactis for obtaining low-fructan bread. The addition of sucrose, which unlike maltose is fermented by Kluyveromyces lactis, or the glucose releasing enzyme amyloglucosidase in the dough both resulted in over 90% removal of fructan. Furthermore, the loaf volumes were comparable to those obtained with S. cerevisiae. Although some of the volatile flavor compounds were present at different levels than in the S. cerevisiae leavened bread, the breads could not be discerned by sensory analysis. Despite that fact that fructose and glucose levels were low when sucrose was added, the authors suggested that glucose addition should be adjusted in order to prevent fructose accumulation. In the case of amyloglucosidase addition, bread fructose content was high (2%), but that of glucose even higher (7%) (Struyf et al., 2018).

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Compared to the typically used yeast-based baking process, sourdough fermentation is a traditional bread-making technique based on the action of lactic acid bacteria (mainly Lactobacillus strains) and yeasts (e.g. Saccharomyces cerevisiae, Candida humilis and Kazachstania exigua). Heterofermentative lactic acid bacteria and yeasts produce carbon dioxide and form flavor compounds. Lactic acid bacteria produce lactic and acetic acids and thereby lower dough pH, which aids in preservation and adds flavor (De Vuyst et al., 2014). Leavening by sourdough techniques requires longer incubation times (from 8 h to over 140 h) than leavening with baker’s yeast (from 0.5 h to 3 h) - an apparent reason why baker’s yeast began replacing sourdough in bakeries during the 19th century (Brandt, 2007; Catzeddu, 2011;

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Menezes et al., 2018). It is possible that the longer leavening time results in more extensive hydrolysis of the cereal carbohydrates, such as FODMAPs, during sourdough fermentation. For instance, lower fructan contents (62% decrease) have been determined in rye breads prepared by sourdough method than in yeast leavened rye breads (32% decrease) (Andersson, Fransson, Tietjen, & Åman, 2009). This is most likely due to the action of bacterial hydrolytic enzymes, but it is also possible that endogenic enzymes are activated at the lower pH in sourdough.

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A strain belonging to Lactobacillus crispatus, a common species of the type II sourdough lactobacilli, has been shown to be capable of fructan hydrolysis (Loponen & Gänzle, 2018; Loponen et al., 2017). A potential problem with the release of fructose from fructan is the capability of many heterofermentative lactic acid bacteria to convert the fructose to mannitol (Kiviharju & Nyyssölä, 2008), which is also a FODMAP compound. However, it has been suggested that the mannitol content can be reduced by mannitol consuming lactobacilli and the choice of suitable raw materials (Loponen & Gänzle, 2018).

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Sourdough rye breads low in FODMAP compounds have been used in two clinical trials to evaluate the effect of their consumption on relieving irritable bowel syndrome symptoms. The results indicated that fermentation in the colon as well as many irritable bowel syndrome symptoms, such as flatulence, cramps and abdominal pain, were reduced in a diet containing low-FODMAP bread in comparison to the diet with regular control bread. Fructan contents were 0.3-0.4% and mannitol contents 0.09-0.1%, whereas in the regular control rye breads they were 1.1-1.2% and 0.26-0.3%, respectively. Although the methods and recipes by which the low-FODMAP breads were produced were not given, the authors stated that the metabolic activity of a Lactobacillus strain present in the sourdough was responsible for the lowered FODMAP contents (Laatikainen et al., 2016; Pirkola et al., 2018). It seems likely that the sourdough strain referred to is the Lactobacillus crispatus sp. isolated from the sourdough seed starter as described in the patent application by the producer of the breads (Fazer bakeries) used in this study (Loponen et al., 2017).

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Sourdough wheat bread produced by long fermentation (over 12 h) has been compared to yeast leavened bread to determine the effect of sour dough baking on the reduction of fructan and α-amylase/trypsin inhibitors (ATIs) content (Laatikainen et al., 2017). ATIs have on the basis of animal and in vitro studies, been hypothesized to promote intestinal inflammation (Junker et al., 2012; Zevallos et al., 2017. Fructan content in sourdough bread was lowered by 74% (to 0.06 g/100 g) in comparison to the yeast leavened bread, and the ATIs were significantly reduced to their monomeric forms. The reduction in FODMAP (fructan) intake due to the consumption of sourdough bread instead of yeast leavened bread by the participants with irritable bowel syndrome was significantly below the minimal difference reported as meaningful in another study by the authors (1.5 g/d, fructans and mannitol)

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(Laatikainen et al., 2016). It was, nevertheless, hypothesized that the synergistic effect of several favorable changes taking place (reduction in ATIs, fructan, additives and gluten) would decrease the inflammation marker levels and gastrointestinal symptoms. However, the hypothesis was not confirmed by the results and no significant differences could be detected. The authors concluded that large scale clinical studies would be needed to establish the possible effects and that results from animal and in vitro studies cannot be directly applied to clinical care (Laatikainen et al., 2017).

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Although bran is an excellent source of phytochemicals and especially dietary fibre, its components are not readily accessible for gastrointestinal digestion. Rye bran has been subjected to a treatment combining enzymatic cell-wall hydrolysis with commercial hydrolase cocktails and fermentation with baker´s yeast. Fructan content of the bran was decreased from 7.5% to 3.4% dw by the combined treatment (Nordlund, Katina, Aura, & Poutanen, 2013).

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α-Galacto-oligosaccharides

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α-Galacto-oligosaccharides (α-GOS) are among the most common polymeric FODMAP sugars found in foods. α-GOS are near ubiquitous in plant seeds, where they accumulate during seed maturation and are degraded during germination. They are hypothesized to play an important role as energy storage molecules that are essential for the early development of the plant (Blöchl, Peterbauer, & Richter, 2007), although this view has also been contested (Dierking & Bilyeu, 2009). There are also strong indications that α-GOS play an important role in the development of drying tolerance during late stage maturation of legume seeds (Bailly et al., 2001). Humans as well as non-ruminant animals lack intestinal α-galactosidase and are therefore unable to digest α-GOS. As major antinutritive compounds in foods, α-GOS are mainly encountered in legumes, although there are significant amounts of α-GOS also in e.g. cashews (Griffin & Dean, 2017) and cabbages (Andersen, Bjergegaard, Møller, Sørensen, & Sørensen, 2005). Considering the increasingly crucial role of legumes, particularly soy, as a source of protein in modern food and feed, the reduction of α-GOS in foods is of great interest.

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In legumes, α-GOS are usually found in contents ranging from less than 1% to approximately 3% (dw) (Naivikul & D´Appolonia, 1978). These α-GOS are predominantly raffinose family oligosaccharides (RFOs), which are α-galactosyl derivatives of sucrose containing one (raffinose), two (stachyose), three (verbascose) or four (ajucose) galactose units connected with α-(1-6) linkages. The chemical structure of the simplest compound of the series, raffinose, is presented in Fig. 1 b. In dicots such as legumes, stachyose and verbascose are the

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most abundant RFOs, while raffinose is the most common RFO sugar found in monocot seeds (Peterbauer & Richter, 2001). In addition to RFOs, legumes can contain lesser amounts of oligogalactosyl derivatives of cyclitols (Obendorf & Kosina, 1974), likely the best-known among them being ciceritol. Somewhat confusingly, the term galacto-oligosaccharide is also used to refer to β-oligogalactosyl derivatives of lactose that are found in milk. In this review, we use the term α-galacto-oligosaccharide (α-GOS) to refer to the raffinose family oligosaccharide (RFO), which are clearly the most common galacto-oligosaccharides in foods.

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Enzymatic removal

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α-Galactosidases (EC 3.2.1.22) catalyze the hydrolysis of galactoses from the non-reducing ends of α-GOS. They have been used in the sugar industry for hydrolyzing α-GOS, which interfere with sucrose crystallization. α-Galactosidases are also used in pre-treatment of animal feeds to improve the digestibility of feedstuffs such as soybean meal in non-ruminant animals. Furthermore, several commercial α-galactosidase containing supplements are available for alleviating flatulence caused by legume-based foods in humans (Katrolia, Rajashekhara, Yan, & Jiang, 2014). At least one commercial enzyme, DS30 (Amano, Japan), is currently on the market for such preparations.

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There are two types of α-galactosidases: those that are active only towards oligomers and those that are active towards both oligomers and galactose polymers (galactomannans, galactoglucomannans). Fungal and yeast α-galactosidases typically have pH optima at 3.5-5.0 and bacterial at 6.0-7.5. Most α-galactosidases characterized exhibit end-product inhibition, limiting the efficiency of enzymatic hydrolysis (Anisha, 2017). Only the α-galactosidase I from Streptomyces griseoloalbus has been reported to tolerate galactose levels of up to 100 mM (Anisha, John, & Prema, 2009). α-Galactosidases are also produced by plants and they are activated during germination, resulting in reduction of the oligosaccharide contents of the seeds (Blöchl et al., 2007). In addition to α-galactosidases, invertases (sucrases, EC 3.2.1.26) are known to have activity towards raffinose (Boddy et al., 1993). They hydrolyze raffinose to melibiose [galactose-α(1-6)-glucose] and fructose. It has been shown that use of invertase together with α-galactosidase results in more extensive hydrolysis of raffinose and stachyose present in soybean and canola flours than hydrolysis with α-galactosidase alone (Slominski, 1994). In addition, levansucrases (EC 2.4.1.10) catalyze the cleavage of fructose from raffinose family α-GOS (Teixeira, McNeill, & Gänzle, 2012). However, levansucrases have also been reported to catalyze the concomitant polymerization of the released fructose to levan (Yamamoto, Iizuka, Tanaka, & Yamamoto, 1985; Andersone, Auzina, Vigants, Mutere, & Zikmanis, 2004), a potential FODMAP.

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The use of α-galactosidases for α-GOS removal from various foods prior to consumption has been widely investigated. In analogy to hydrolysis of lactose from cow milk, the hydrolysis of

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α-GOS from soy milk has been demonstrated in a number of reports both with free αgalactosidases (Cruz & Park, 1982; Gote, Umalkar, Khan, & Khire, 2004; McGhee, Silmaim, & Bagley, 1978; Patil, Mulimani, Veeranagouda, & Lee, 2010; Wang et al., 2014) and with αgalactosidases immobilized to various supports, such as calcium alginate (Rajan & Nair, 2010), polyvinyl alcohol (Patil & Mulimani, 2008), κ-carrageenan (Girigowda & Mulimani, 2006), chitosan and amberlite (Singh & Kayastha, 2012).

402 403 404 405 406 407 408 409

An overview of enzymatic removal of α-GOS from different legume flours is shown in Table 4. In most cases, enzymatic treatment compares favorably with other treatments such as soaking, autoclaving, cooking and germination. It should, however, be noted that enzymatic oligosaccharide hydrolysis has been carried out with legume flours as the substrates whereas whole beans have been used in the alternative treatments. The obvious benefit of the enzymatic treatment is, nevertheless, that heating and large volumes of water used in soaking followed by cooking can be avoided.

410 411

Removal by fermentation

412 413 414 415 416 417

Considering the relative abundance of α-galactosidase expressing microbes, particularly bacteria and fungi, the removal of α-GOS by fermentation represents an attractive alternative. In addition to α-GOS, fermentative processes can also degrade other antinutritional factors (Granito et al., 2002) and impart novel flavors (Gu et al., 2018) or textures (Xu, Wang, et al., 2017).

418 419 420 421 422 423 424 425 426 427 428 429 430 431 432 433 434 435

Soybean is globally the most important commercial plant containing high levels of α-GOS. Soybean originates from East Asia, where it has been traditionally fermented using both bacteria and fungi to produce a diverse range of dishes (O’Toole, 2016). Fermentation of soy using Aspergillus oryzae dates back at least 2000 years and is used in the production of, for example, soy sauce and miso paste (Machida, Yamada, & Gomi, 2008). Fermentation using Actinomucor elegans is used in the production of furu in China (Lin, Sirisansaneeyakul, Wang, & McElhatton, 2016). In Indonesia, Rhizopus oligosporus is used to produce tempeh (Rehms & Barz, 1995) and Neurospora sitophila is used to produce oncom (Fardiaz & Markakis, 1981), both cake-like products containing soy. Fermentation using Bacillus subtilis var. natto is used in Japan and other countries to produce nattō and similar dishes with a stringy consistency (Kanno, Takamatsu, Takano, & Akimoto, 1982). A wide range of lactic acid and other bacteria are involved in the production of the Chinese delicacy stinky tofu (Gu et al., 2018). Many of the organisms traditionally used for fermenting soy are capable of producing α-galactosidases, so it is not completely surprising that analysis by Monash University found fermented tempeh and soy sauce to be low in FODMAP, while soy beans were high in FODMAP (Iacovou, Tan, Muir, & Gibson, 2015).

12

436 437 438 439 440 441 442 443 444 445 446 447

In some cases, the reduction of α-GOS in traditional fermented soybean products has been studied in more detail. A large variation in the ability to degrade α-GOS was found between different Rhizopus spp. producing tempeh (Rehms & Barz, 1995), with some species including R. oligosporus NRRL-2710 not degrading α-GOS at all, while other Rhizopus spp. removing practically all α-GOS during the course of fermentation. R. oligosporus 2770 did not degrade α-GOS in tempeh fermentation studies on soy and peas (Nowak & Szebiotko, 1992). Fardiaz & Markakis (1981) also found R. oligosporus slow to degrade α-GOS, but found oncomproducing Neurospora sitophila to rapidly consume these sugars. Kanno et al. (1982) followed the decrease in α-GOS during the production of natto and found 7.49 wt% α-GOS in the starting material while only 1.75 wt% remained in the matured product. Moy & Chou, (2010) found significant reduction in α-GOS during the production of the fermented tofu product sufu.

448 449 450 451 452 453 454 455 456 457 458 459

Beyond East Asia, several traditional fermented dishes with potentially lowered α-GOS content are also prepared. A number of fermented dishes containing legumes are produced in India, such as idli, dosa, ambali, dhokla, kinema, tungrybai and hawaijar (Sathe & Mandal, 2016). Idli, a lactic acid fermented cake containing black gram (Phaseolus mungo), has been shown to have 30% lower α-GOS than the unfermented batter (Reddy, Sathe, Pierson, & Salunkhe, 1982). Locust beans (Parkia biglobosa) are traditionally fermented in West Africa to produce a product variably known as dawadawa, sikomu, iru or eware. The production process has been shown to dramatically reduce α-GOS content (Odunfa, 1983). In Burkina Faso, pearl millet (Pennisetum glaucum) is converted into a gruel known as ben-saalga through lactic acid fermentation, which has been shown to result in over 80% reduction in raffinose content (Tou et al., 2006).

460 461 462 463 464 465 466 467 468 469

Most studies on fermentation using filamentous fungi have focused on traditionally developed and accepted dishes. This might be due to the fact that regulatory approval for novel foods prepared using this class of organisms can be difficult (Leuschner et al., 2010). Conversely, many bacterial species are considered probiotics and approved for food use. Indeed, there are many studies not relying on traditional fermentations that have looked at the impact of lactic acid fermentation on the α-GOS content of whole legumes, legume flours and legume broths, as summarized in Table 5. A recent study found up to 75% of tested probiotic bacteria capable of fermenting the major forms of α-GOS (Zartl et al., 2018), highlighting the potential of this approach.

470 471 472 473 474 475

The use of lactic acid fermentation to reduce α-GOS content in soy milk has been recognized for a long time. A limiting factor in this approach can be that the fermentation of the predominant sugar in soy milk, sucrose, leads to a decrease in pH, which then inhibits the consumption of α-GOS (Mitall & Steinkraus, 1979). Accordingly, Inoguchi et al. (2012) reported only consumption of glucose and sucrose in soy milk fermented for 12 hours using a

13

476 477 478 479 480 481 482 483

Kefir starter. Nonetheless, complete or near complete removal of raffinose and stachyose from soy milk through fermentation using specific lactic acid bacteria has been achieved in several studies (Baú, Garcia, & Ida, 2015; Liu, Li, Yang, Liang, & Wang, 2006; Scalabrini, Rossi, Spettoli, & Matteuzzi, 1998; Yoon & Hwang, 2008). Promising results were also achieved on a broth prepared from Nigerian bean varieties (Adewumi & Odunfa, 2009). Other studies on legume broths reported lower decreases in α-GOS content ranging from about 15% to 40% (Battistini et al., 2018; Feng, Saw, Lee, & Huang, 2008; Omogbai, Ikenebomeh, & Ojeaburu, 2005; Ziarno, Zaręba, Maciejak, & Veber, 2019).

484 485 486 487 488 489 490 491 492 493 494 495 496 497

Lactic acid fermentation has also been applied to legume flours and entire seeds. Granito and co-workers demonstrated complete or near complete removal of α-GOS from whole beans through lactic acid fermentation (Granito & Álvarez, 2006; Granito et al., 2002). Approximately 70% of α-GOS was also removed from whole soybeans through fermentation with Lactobacillus plantarum (Adeyemo & Onilude, 2014). Complete or near complete removal of α-GOS has been observed in several studies on the fermentation of faba bean flour using various lactic acid bacteria (Rizzello, 2019; Xu, Coda, Shi, Katina, & Tenkanen, 2017; Xu et al., 2017), while another study found only 40% removal (Verni et al., 2017). Complete or near complete removal has also been observed for lentil (Frias, Díaz-Pollan, Hedley, & VidalValverde, 1996), cowpea (Doblado, Frias, Munoz, & Vidal-Valverde, 2003), pigeon pea (Torres, Frias, Granito, & Vidal-Valverde, 2006) and chickpea (Montemurro, Pontonio, Gobbetti, & Giuseppe, 2019) flours. Mixed results regarding α-GOS removal were seen with flour prepared from Australian sweet lupin (Kaczmarska, Chandra-hioe, Zabaras, Frank, & Arcot, 2017).

498 499 500 501 502 503 504 505 506 507 508 509 510 511 512

When discussing removal of α-GOS via fermentation, it is important to note that αgalactosidase is not the only enzyme that may be degrading the sugars. Many invertases (and fructansucrases, see above) are able to cleave the final fructose unit of α-GOS. Most of the studies on α-GOS removal reviewed here only quantify the decrease in raffinose-family oligosaccharides and do not mention or quantify melibiose, manninotriose and manninotetraose, the products of invertase catalyzed hydrolysis on raffinose, stachyose and verbascose, respectively. For example, significant formation of melibiose, manninotriose and manninotetraose has been noted when fermenting faba and soybean flours using Leuconostoc mesenteroides DSM 20343 (Xu, Coda, Shi, Katina, & Tenkanen, 2017). Others have also noted the formation of these sugars through fermentation with lactobacilli as well as analyzed their hydrolysis by α-galactosidases produced by the strains (Teixeira, McNeill, & Gänzle, 2012). Lactobacilli can also produce other types of α-GOS through transglycosylation (Black et al., 2012). It is therefore possible that the decrease in α-GOS content may be significantly overestimated in some cases.

513 514 515

Removal by germination

14

516 517 518 519 520 521 522 523 524 525 526

As discussed previously, germination of seeds is associated with a decrease in their α-GOS content, and this process may be crucial for the early development of the plant (Blöchl et al., 2007). Therefore, germination offers a way of decreasing α-GOS content using the endogenous enzymes of the seed in a process analogous to the malting of cereals. In addition to α-GOS, germination can alter the content of other nutrients such as vitamins (Urbano et al., 2005; Vidal-Valverde et al., 2002), phytates (Goyoaga et al., 2011; Mubarak, 2005; VidalValverde et al., 2002), protein (Ribeiro et al., 2011; Urbano et al., 2005) and fat (Mubarak, 2005). As with fermentation, germination of legumes is traditionally used in some South and East Asian cuisines (Kadlec, Dostálová, Bernášková, & Skulinová, 2008; Vidal-Valverde et al., 2002).

527 528 529 530 531 532 533 534

The effect of germination on the α-GOS content of a wide variety of legumes has been studied, as summarized in Table 6. The list of studied legumes is extensive and covers common bean, soybean, faba bean, chickpea, lentil, pea, cowpea, lima bean, pigeon pea, African yam bean, jack bean, mung bean, mucuna, dolichos, ricebean and lupin. In general, germination has been found to be very efficient at removing α-GOS from legumes. With few exceptions, complete or near complete elimination of α-GOS through germination has been reported for all the studied legumes.

535 536 537 538 539 540 541 542 543 544 545 546

Germination times ranging from half a day up to nine days have been studied (Goyoaga et al., 2011), but more commonly the germination times have been from 3 to 6 days. Typically, efficient removal of α-GOS from legumes through germination is a process that requires several days. In most cases, germination has been carried out in the dark, but in a number of studies, either continuous or discontinuous lighting has also been applied. No major differences in the decrease in α-GOS content or composition of beans, lentils and peas were found in germination under light and dark conditions (Vidal-Valverde et al., 2002). MartínCabrejas et al. (2008) studied changes in composition in cowpea, jack bean, mucuna, dolichos and soybean during germination, and found only very minor differences in α-GOS content when the legumes were germinated in the dark, with a 12-hour light-dark cycle or with continuous illumination.

547 548 549 550 551 552 553 554 555

Germination temperatures used generally range from 20 to 28°C, with the exception of the study by Kaur & Kawatra (2000), where 37°C was used. When response surface methodology was applied to determining the effect of soaking time, germination time and temperature on the composition of cowpeas, only minor differences in α-GOS content were found when the germination temperature was varied between 20 and 30°C (Wang, Lewis, Brennan, & Westby, 1997). As expected, germination time had a strong negative correlation with α-GOS content in the cowpeas. The combination of a short germination period (16 hours) followed by cooking of pigeon pea (Cajus cajan) was found to remove 71.7% raffinose, 76.2% stachyose and 74.0%

15

556 557 558

verbascose (Devindra, Rao, Krishnaswamy, & Bhaskar, 2011). Germination has also been found effective at removing α-GOS from other seeds such as canola (Barthet & Daun, 2005), amaranth (Colmenares De Ruiz & Bressani, 1990).

559 560 561

Lactose

562 563 564 565 566 567 568 569 570

Lactose is the main carbohydrate of mammalian milk, and it is present in bovine milk at approximately 5 g/L. It is a disaccharide consisting of galactose and glucose molecules linked by a β(1-4) glycosidic bond (Fig. 1 c). The hydrolysis of lactose to its monosaccharide components is catalyzed by enzymes belonging to β-galactosidases (3.2.1.23). While βgalactosidases are widely distributed in nature, the plant and animal variants (excluding intestinal ones) have been claimed to have low activity towards lactose. Lactose hydrolyzing (lactase) activity is mainly limited to the intestinal brush border of mammals and to microbes (Husain, 2010; Mahoney, 1997).

571 572 573 574 575 576 577 578 579 580 581 582 583

Majority of human adults are more or less intolerant towards lactose, because of decreased intestinal lactase activity. There are four types of lactase deficiency: primary, secondary, congenital, and developmental. After weaning from breast milk the intestinal lactase activity of most mammals typically decreases and the ability to digest lactose declines (primary deficiency). However, in some populations in Northern Europe and in West Africa with a history of cattle husbandry, the continued production of lactase, so-called lactase persistence, in adulthood is more common. Lactase persistent individuals may become lactase deficient due to injuries of the small bowel caused by infections, inflammation, other diseases, or surgery (secondary deficiency). Congenital lactase deficiency is a rare genetic disorder of newborns with in little or no lactase production. Developmental lactase deficiency is a temporary conditions of premature infants, which typically improves as the mucus of the small intestine develops (Bhatnagar & Aggarwal, 2007; Deng, Misselwitz, Dai, & Fox, 2015).

584 585

Enzymatic removal

586 587 588 589 590 591 592 593

Although most humans tolerate moderate amounts of milk, considerable effort has been taken by the dairy industry to develop low-lactose milk products for lactose intolerant consumers (Deng et al., 2015). Methods for reducing lactose content of milk products are well-documented in several reviews (Harju, Kallioinen, & Tossavainen, 2012; Jelen & Tossavainen, 2003; Mahoney, 1997; Panesar, Panesar, Singh, Kennedy, & Kumar, 2006; Shukla & Wierzbicki, 1975) and only a summary of this field is given here. The low-lactose and hydrolyzed-lactose milk products, which have been on the market for decades, even before

16

594 595

the term FODMAP was coined, are the first examples of food products, where these compounds have been removed by bioprocessing.

596 597 598 599 600 601 602

Lactases have been commercially available for lactose hydrolysis from the 1970’s. Commercial sources include enzymes from yeasts, fungi and bacteria. The fungal enzymes, produced with e.g. Aspergillus spp., typically have optima for activity at acidic range and can therefore be used for processing acid whey (a by-product of e.g. cottage cheese manufacturing). The lactases from yeasts such as Kluyveromyces sp. and bacteria such as Bacillus sp. on the other hand are active at neutral pH and therefore suitable for treating milk (Panesar et al., 2006).

603 604 605 606 607 608 609 610 611 612 613 614 615

Lactose hydrolysis can be carried out simply by adding lactase to pasteurized milk followed by either overnight incubation at refrigerator temperatures or by shorter incubation at 35 °C. When high enough extent of lactose hydrolysis is achieved, milk is ultrapasteurized to inactivate the enzyme. In a variation of the process, a filter-sterilized lactase preparation is added to ultrapasteurized milk, and the mixture is incubated for several days at room temperature. Since hydrolysis takes place under sterile conditions, the incubation time can be longer without the risk of microbial contamination. Hence, only small amounts of the enzyme are needed (Harju et al., 2012; Mahoney, 1997). Hydrolysis of lactose by lactases results in increased sweetness because of the galactose and glucose released. In some products this is useful, since the amount of added sugar can be reduced. On the other hand, in heat-treated products Maillard reactions may be intensified, since both glucose and galactose are reducing sugars (Harju et al., 2012).

616 617 618 619 620

Valio Ltd. (Finland) and Lactaid (USA) were the first companies to start industrial production of lactose hydrolysed milk in the 1980’s, after which several different hydrolyzed lactose products, such as cream, yoghurt, buttermilk, ice cream and cottage cheese have become available for the consumers (Harju et al., 2012).

621 622 623 624 625 626 627 628 629 630 631 632 633

The use of immobilized enzymes enables reuse and continuous processes resulting in reduction in enzyme costs. Although immobilization of lactases by adsorption, entrapment and covalent binding on various carriers has been studied extensively (Husain, 2010; Panesar et al., 2006), there are only few industrial applications of these techniques for milk processing. For instance, a lactase from Kluyveromyces lactis has been immobilized in microcavities of cellulose triacetate fibres and an Aspergillus oryzae lactase on the surface of an amphoteric ion-exchange resin. These K. lactis and A. oryzae immobilizates have been used commercially for milk treatment in Italy and Australia, respectively (Honda, Kako, Abiko, & Sogo, 1993). Apparently the main problems related to repeated operations using immobilization are microbial contamination of the milk, adherence of protein on the biocatalyst and channeling of the biocatalyst bed (Panesar et al., 2006).

17

634 635 636 637 638 639 640 641 642 643 644 645 646 647 648 649

An alternative for simple hydrolysis of milk lactose by lactases is based on chromatographic separation of bulk of the lactose from milk minerals and protein. When the latter fraction is combined with lactase-hydrolyzed milk, a milk-product containing less than 0.01% (w/w) lactose, but with sweetness similar to ordinary milk, is achieved. This type of process, introduced by Valio Ltd. Finland, has been further refined using membrane techniques instead of chromatography. A lactose and mineral containing fraction is first separated from milk by ultrafiltration. This fraction is then nanofiltered to remove the lactose, and the permeate with the minerals is concentrated by reverse osmosis. When the concentrate is combined with the protein-rich ultrafiltration retentate and the residual lactose is hydrolyzed by lactase treatment, a lactose-free milk product without extra sweetness is obtained (Harju et al., 2012; Jelen & Tossavainen, 2003). Ultrafiltration has also been applied individually for decreasing the lactose content to a suitable level and applying lactase for hydrolyzing the remaining lactose to achieve sweetness matching that of normal milk (Lange, 2005). However, in this case the mineral content is decreased, which may have an effect on the taste. After these pioneering examples, several processes based on membrane separation and lactase treatment have been described (Harju et al., 2012).

650 651

Removal by fermentation

652 653 654 655 656

Microbes can easily contaminate and spoil raw milk. This may lead to compromised safety if pathogenic micro-organisms are involved. The traditional way to preserve milk has been to use safe lactic acid bacteria for fermenting the lactose to lactate and thereby acidifying the product.

657 658 659 660 661 662 663 664 665 666 667 668 669 670

Lactic acid bacteria take up lactose in free form by a permease system or as lactose-phosphate by a lactose specific phosphoenolpyruvate-dependent sugar phosphotransferase system (PTS). If lactose enters the cells via a permease, it is first cleaved to glucose and galactose by a lactase. Glucose is phosphorylated to glucose-6-phosphate and enters glycolysis and galactose is phosphorylated to galatose-1-phosphate, which is then converted to glucose-6phosphate for further catabolism. If lactose is phosphorylated and transported by the PTS system, it is split into glucose and galactose-6-phosphate. Glucose is again metabolized by glycolysis and galactose-6-phosphate via the tagatose-6-phosphate pathway. Of the common dairy starters Streptococcus thermophilus, which is used for manufacturing yogurt, has the permease system, whereas Lactococcus lactis, used in cheese production, transports lactose via the PTS system. However, S. themophilus strains typically secrete galactose into the medium instead of fermenting it (Axelsson, 1988). In any case, lactose metabolism leads to rapid acidification of the medium.

671 672 673

During yellow cheese manufacturing most of the lactose ends up in whey after curdling and straining. The lactose remaining in the solid cheese phase is consumed by fermentation,

18

674 675 676

making the final product virtually lactose free. Consumption of dairy as cheese is, therefore, popular in central and southern Europe, where lactose intolerance is highly prevalent (Harju et al., 2012).

677 678 679 680 681 682 683 684 685 686 687 688

Fermentation is also used for the production of spoonable or drinkable milk products such as yogurt, buttermilk, kefir and ropy milk. As the result of fermentation, these products contain approximately between 20 to 40% less lactose than unfermented milk (Ohlsson et al., 2017), which may make them better tolerated than milk. Although a considerable proportion of lactose therefore remains intact, products such as yogurt are widely used in eastern Europe, where lactose intolerance is nevertheless relatively common (Harju et al., 2012). An explanation to this apparent contradiction is that the live bacterial cultures present in the product provide a source of lactase for lactose hydrolysis. Lactases are protected by the bacterial cells and the buffering capacity of the fermented milk under the acidic conditions of the stomach. The lactases are again functional in the small intestine, where the pH is higher, aiding in lactose digestion (Savaiano, 2014).

689 690

Sugar alcohols and fructose

691 692 693 694 695 696 697 698

Sugar alcohols, such as the monosaccharide polyols mannitol (Fig. 1 e), sorbitol (Fig.1 f), xylitol and erythritol, and the disaccharide-derived maltitol, lactitol and isomalt, are used as lowcalorie sweeteners. They are usually manufactured chemically by catalytic reduction of sugars. However, mannitol, sorbitol, xylitol and erythritol are also naturally found in some foods, although in most cases in relatively small amounts. In addition to sweetening foods such as confectionary products, soft drinks and baked goods etc., sugar alcohols give texture and bulk to the products.

699 700 701 702 703 704 705

With the exception of erythritol, sugar alcohols are typically incompletely absorbed in the small intestine, which can trigger gastrointestinal symptoms (Grembecka, 2015; Mäkinen, 2016). Although erythritol is relatively well absorbed, its effects on patients with IBS have to our knowledge not been investigated. Since sugar alcohols are used widely as food additives, they may become a significant source of FODMAPs in the diet. Their removal by enzymatic or other means from such products is obviously not relevant.

706 707 708 709 710 711 712 713

In nature, sugar alcohols are mostly found at relatively low levels, and in a limited number of products. Xylitol is present in small amounts (< 1% dw) in some fruits such as plums, strawberries and raspberries, as well as in vegetables such as cauliflower, lettuce and eggplant (Jaffe, 1978). Sorbitol is a main FODMAP compound in some fruits such as pears, apples and peaches, where its concentration has been reported to range between 0.5 and 6.0 % fresh weight. It is also present in some vegetables, but in smaller amounts. Mannitol is found in fruits, such as watermelon and peach as a minor component. Mushrooms and cauliflower

19

714 715

have been reported to contain relatively high levels of mannitol, at approximately 3 % fresh weight (Muir et al., 2009) (Table 1).

716 717 718 719 720 721 722 723

As discussed above, the fructose present in sourdough may be converted to mannitol by mannitol dehydrogenases of heterofermentative lactobacilli, but its concentration can be reduced by mannitol consuming strains (Loponen & Gänzle, 2018). Mannitol production from fructose can also take place in other food products, such as sauerkraut and kimchi, fermented with lactic acid bacteria (Sinha, Hui, Evranuz, Siddiq, & Ahmed, 2010). To our knowledge, there are no reports on attempts to remove sugar alcohols from foods by separation, enzymatic conversion or other biological means to avoid their harmful gastrointestinal effects.

724 725 726 727 728 729 730 731 732 733

Fructose (Fig. 1 d) is a ubiquitous monosaccharide found in a wide variety of fruits and vegetables either in free form, or as a part of sucrose, in which it is linked with glucose. As discussed above, fructose is regarded as FODMAP, when it is present in excess to glucose. This is because intake of glucose together with fructose considerably facilitates the absorption of the latter. The capacity to absorb fructose varies within the population. However, it has been estimated that approximately half of US population is unable to absorb 25 g of pure fructose (Gibson et al., 2006). An excess of fructose to glucose is typical for instance in pears, apples and juices produced from them (ranging from 2 to 8 % fresh weight). (Rumessen, 1992) (Table 1).

734 735 736 737 738 739 740 741 742 743 744

Fructose consumption has been increasing for decades, especially in the U.S., because of growing use of high-fructose corn syrup (HFCS), which is an alternative to the more expensive sucrose. HFCS-sweetened beverages have typically fructose-to-glucose ratios of approximately 60:40, with total sugar contents of around 100 g/L. Some fruit juices, sweetened with fruit juice concentrates instead of HFCS, contain even higher concentrations of fructose and have higher fructose-to-glucose ratios. These popular beverages are a major source of excess fructose, which in addition to being FODMAP, is linked to metabolic disorders (Rumessen, 1992; Walker, Dumke, & Goran, 2014). As with products with added sugar alcohols, omitting these products from the diet is the simplest solution to avoid gastrointestinal symptoms.

745 746 747

Conclusions and future perspectives

748 749 750 751 752 753

Food FODMAP content can be reduced significantly by bioprocessing by enzymes, fermentation and germination. Enzyme-aided treatments are more specific and easier to control than those based on fermentation and germination. With specific enzyme preparations, side reactions taking place during fermentation and germination can be avoided. For example, during sourdough-type fermentation, in addition to changes caused by

20

754 755 756 757 758 759 760 761 762 763 764 765

microbial enzymes, acidification of the raw materials activates several endogenous enzymes (e.g. proteases, xylanases) that affect the food matrix (Boskov Hansen et al., 2002), induce formation of flavours (Heiniö et al., 2016), and cause changes in nutritional quality (Poutanen, Flander, & Katina, 2009). Germination is a relatively slow process, taking days (Matella et al., 2006), and results in numerous changes in the raw materials due to breakdown of seed components for energy (Abudu & Akinyele, 1990). Generally, in the bioprocessing treatments targeting FODMAP reduction, it is important to control the possible side reactions to ensure that, for example, formation of new FODMAP components and off-flavours or breakdown of structure building polymers do not take place. Bioprosessing may in some cases lead to conversion of the target FODMAPs to other FODMAPs. For instance, fructanase treatment releases fructose and during fermentation mannitol may be produced. In these cases, alternative methods or further processing can considered.

766 767 768 769 770 771 772 773 774 775 776 777 778 779

Nutritional quality, and specifically dietary fibre content, are important issues to consider when FODMAP content of foods is reduced. Treatment of foods with enzymes specific for their FODMAP substrates does most likely not affect the vitamin content or the bioavailability of minerals significantly. Germination may either decrease or increase the vitamin content, or have no effect on it. For instance, germination of some legumes has been reported to increase vitamin C, riboflavin, niacin and biotin levels, but decrease the folic acid content. Thiamin concentrations were reported in these studies to either remain the same or increase, while the concentration of pantothenic acid was unaffected (Nkhata, Ayua, Kamau, & Shingiro, 2018; Vanderstoep, 1981). Fermentation may also have different effects on the vitamin levels depending on the fermenting microbes in question. Some fermenters produce vitamins, for instance Streptococcus thermophilus and propionibacteria are folate and vitamin B12 synthesizers, respectively. Some microbes have no effect on vitamins and some, such as folate utilizing lactobacilli, consume them during growth (Walther & Schmid, 2017).

780 781 782 783 784 785 786 787 788 789

Binding of mineral nutrients to phytate, polyphenols and oxalate impairs their bioavailability. Germination increases the activities of phytate degrading enzymes, resulting in liberation of minerals, such as iron, calcium and magnesium (Luo, Xie, Jin, Wang, & He, 2014; Nkhata et al., 2018). Fermentation has been reported to increase the bioavailability of minerals such a calcium and iron, presumably because of degradation of phytate and oxalate. However, fermentation may also result in release of mineral binding tannins and phenols, with opposing effects. Degradation of components such as fibres, and starch during fermentation, on the other hand, leads to loosening of the matrix structure and better bioavailability (Nkhata et al., 2018).

790 791 792 793

FODMAP compounds, especially α-GOS and fructan are also dietary fibre components. Dietary fibre intake has been associated with health-benefits (Jefferson & Adolphus, 2019) and both the Western and low-FODMAP diet are characterized by low dietary fibre content. Although

21

794 795 796 797 798 799

FODMAP reduction may decrease the dietary fibre content of the food, applying specific tools to reduce only the FODMAP content of foods would allow consumption of a wider variety of foods by gastrointestinally sensitive consumers, and make it easier for them to eat a varied dietary fibre-rich diet. Furthermore, it is important to understand the level of FODMAP reduction needed, i.e. to elaborate on the levels of FODMAPs that are tolerated by specific consumers segments experiencing the discomfort.

800 801 802 803 804 805 806 807 808 809 810 811 812 813 814 815 816 817 818 819 820 821 822 823 824 825 826 827 828 829 830 831

In general, more systematic clinical studies are needed to identify specific FODMAP compounds and their tolerance levels in different groups. As shown in this review, there are some reports on physiological consequences of fructan degradation in breads, but for instance with α-GOS, clinical studies on the impact of α-GOS reduction in foods on intestinal discomfort are very rare. Indeed, estimates on the target FODMAP contents and tolerated intakes in both general population and specific patient groups are needed. Furthermore, interindividual variation should be investigated and methods to diagnose and monitor gastrointestinal discomfort developed further. Related to this, more knowledge about the interplay of non-digestible food compounds and gut microbiota should be generated, as this is an important aspect of health and wellbeing. Avoidance of whole food groups because of FODMAP “fear” may lead to sub-optimal diets. The low FODMAP diet is a diet therapy for individuals with a functional gut disorder (IBS). It is not a diet suitable for healthy population. Regarding the future of bioprocessing tools, new enzymes, starter cultures and processes should be developed, e.g. enzymes with required specificity, pH range and temperature stability. FODMAP content can be reduced in the course of ingredient manufacturing, e.g. during wet separation processes in plant protein production, or during food processing and manufacturing (in situ FODMAP reduction). Furthermore, developing cultivars with low FODMAP content by plant breeding is another interesting option. An important aspect to keep in mind is that food products are also supplemented with FODMAPs. For instance, inulin is often added into liquid or semi-solid foods to improve the texture of the products. Therefore, finding replacing performance ingredients, for example to inulin and some sugar alcohols, is of importance. FODMAP reduction can contribute to the transition towards more plant-based diets. However, application of bioprocessing tools for treating various raw materials and food matrices requires careful analysis and optimization to enable production of foods and diets optimal from nutritional, sensory and tolerance viewpoints.

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Acknowledgement

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This work was partly funded by VTT SB project: FODMAP – Reducing FODMAP content in plant-based foods and ingredients. 2018-2019.

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synthesis of exopolysaccharides by Leuconostoc spp . and Weissella spp . and their rheological impacts in fava bean flour. International Journal of Food Microbiology, 248, 63–71. https://doi.org/10.1016/j.ijfoodmicro.2017.02.012. Yamamoto, S., Iizuka, M., Tanaka, T., & Yamamoto, T. (1985). The mode of synthesis of levan by Bacillus subtilis levansucrase. Agricultural and Biological Chemistry, 49, 343–349. https://doi.org/10.1080/00021369.1985.1086672. Yoon, M. Y., & Hwang, H. J. (2008). Reduction of soybean oligosaccharides and properties of α-d-galactosidase from Lactobacillus curvatus R08 and Leuconostoc mesenteriodes JK55. Food Microbiology, 25, 815–823. https://doi.org/10.1016/j.fm.2008.04.008. Yun, J. W., Kang, S. C., & Song, S. K. (1996). Mannitol accumulation during fermentation of Kimchi. Journal of Fermentation and Bioengineering, 81, 279–280. https://doi.org/10.1016/0922-338X(96)82224-0. Zartl, B., Silberbauer, K., Loeppert, R., Viernstein, H., Praznik, W., & Mueller, M. (2018). Fermentation of non-digestible raffinose family oligosaccharides and galactomannans by probiotics. Food and Function, 9, 1638–1646. https://doi.org/10.1039/c7fo01887h. Ziarno, M., Zaręba, D., Maciejak, M., & Veber, A. L. (2019). The impact of dairy starter cultures on selected qualitative properties of functional fermented beverage prepared from germinated white kidney beans. Journal of Food & Nutrition Research,58, 167–176. Zevallos, V. F., Raker, V., Tenzer, S., Jimenez-Calvente, C., Ashfaq-Khan, M., Rüssel, N., … Schuppan, D. (2017). Nutritional Wheat Amylase-Trypsin Inhibitors Promote Intestinal Inflammation via Activation of Myeloid Cells. Gastroenterology, 152, 1100-1113.e12. https://doi.org/10.1053/j.gastro.2016.12.006. 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.

36

1468

Figure legends

1469 1470 1471 1472 1473 1474

Fig. 1. Examples of FODMAP molecules. (a) Fructan with fructose units linked via β(2-1) glycosidic bonds. The number of fructose units (in brackets) varies. (b) Raffinose, the simplest sugar of the raffinose family oligosaccharides containing one α(1-6)-linked galactosyl moiety. (c) Lactose, composed of galactose and glucose linked by a β(1-4)-glycosidic bond. (d) Fructose. (e) Mannitol and (f) Sorbitol.

Table 1. Examples of FODMAP containing foods (g/100 wet weight).1 Food

Galactooligos

Fructans

Lactose

Fructose in excess to glucose

Sorbitol

Mannitol

Reference

Red kidney beans, boiled

1.4

0.54

na

nd

nd

nd

(Biesiekierski et al., 2011)

Haricot beans, boiled

1.1

0.26

na

nd

nd

nd

(Biesiekierski et al., 2011)

Lima beans, boiled

1.3

0.29

na

nd

nd

nd

(Biesiekierski et al., 2011)

Red lentils, boiled

0.46

0.14

na

nd

nd

nd

(Biesiekierski et al., 2011)

Split peas, boiled

1.9

0.73

na

0.01

nd

nd

(Biesiekierski et al., 2011)

Chickpeas, boiled

1.3

tr

na

nd

nd

nd

(Muir et al., 2009)

Textured soy protein

5.5

1.1

nd

nd

nd

nd

(Tuck et al., 2018)

Soy yogurt, plain

0.46

0.14

nd

nd

nd

nd

(Tuck et al., 2018)

Wheat germ

3.9

2.5

nd

0.07

0.03

nd

(Tuck et al., 2018)

Jerusalem artichoke

na

16-20

na

na

na

na

Garlic Onion Leek Asparagus Banana Rye bread (sourdough) Rye bread (sourdough, yeast) Whole wheat bread

na na na na na na

9.8-16 1.1-7.5 0.5-7.1 2.0-3.0 0.7 1.1

na na na na na na

na na na na na na

na na na na na na

na na na na na 0.3

na

1.9

na

na

na

na

(Whelan et al., 2011)

0.2

0.68

na

0.16

tr

tr

(Biesiekierski et al., 2011)

Whole wheat pitta bread

na

0.74

na

na

na

na

(Whelan et al., 2011)

Bovine milk Yogurt

na na

na na

4.1-5.0 2.9-4.2

na na

na na

na na

(Gille et al., 2018) (Gille et al., 2018)

Cottage cheese

na

na

1.8

na

na

na

(Gille et al., 2018)

Popular sodas

na

na

nd

2.1-2.4

na

na

(Walker, Dumke, & Goran, 2014)

Pear

nd

nd

na

2.3-5.0

2.3-6.0

nd

(Muir et al., 2009)

Apple

nd

nd

na

0.14-0.73

0.70-0.83

nd

(Muir et al., 2009)

Peach

nd

nd/tr

na

0 - 4.2

0.68-0.99

0-0.52

(Muir et al., 2009)

Blackberry

nd

tr

na

nd

4.6

nd

(Muir et al., 2009)

Cauliflower

nd

nd

na

nd

nd

3.0

(Muir et al., 2009)

Button mushrooms

nd

0.27

na

nd

0.11

2.6

(Muir et al., 2009)

Kimchi

na

3.9-4.1

na

nd

na

0.4-0.5

(Yun, Kang, & Song, 1996)

Wakame flakes

nd

0.04

nd

nd

nd

2.1

(Tuck et al., 2018)

1

nd: analyzed, but not detected, na: not analyzed, tr: trace.

(Van Loo, Coussement, De Leenheer, Hoebregs, & Smits, 1995) (Van Loo et al., 1995) (Van Loo et al., 1995) (Muir et al., 2007) (Van Loo et al., 1995) (Van Loo et al., 1995) (Laatikainen et al., 2016)

Table 2. FODMAP hydrolyzing enzymes. Enzyme Exoinulinase

EC number EC 3.2.1.80

Substrate Fructan

Endoinulinase

EC 3.2.1.7

Fructan

Invertase

EC 3.2.1.26

Fructan

Levanase

EC 3.2.1.65

Levan type of fructan

α-Galactosidase

EC 3.2.1.22

Invertase

EC 3.2.1.26

Galactooligosaccharides Raffinose1

β-Galactosidase

EC 3.2.1.23

Lactose

1

Raffinose is a galacto-oligosaccharide

Target glycosidic bond Terminal β(2-1) bonds between fructose units Internal β(2-1) bonds between fructose units Terminal β(2-1) bonds between fructose unists and Terminal β(1-2) bonds between glucose and fructose β(2-6)-bonds between fructose units Terminal α(1-6)-bonds between galactose units Terminal β(1-2) bonds between glucose and fructose β(1-4) bond between galactose and glucose

Reference (Singh & Singh, 2017) (Singh & Singh, 2017) (Wang & Li, 2013)

(Chaudhary, Gupta, Gupta, & Banerjee, 1996) (Katrolia, Rajashekhara, Yan, & Jiang, 2014) (Boddy et al., 1993) (Mahoney, 1997)

Table 3. Degradation of fructans from foods by bioprocessing Substrate

Method

Reduction

Reference

Wheat bread

Baker´s yeast and Lb. crispatus fructanase, fermentation 120 min, 37 °C

Bread without fructanase 0.25% (dw), Enzyme treated bread 0.05% (dw)

(Loponen et al. 2017)1

Wheat bread

Baker´s yeast, 25 min kneading, 100 min fermentation (temperature not given)

2.0 g/100 g (dw) in flours, 0.76 g/100 g in bread

(Knez, Abbott, & Stangoulis, 2014)

Wheat bread

Baker´s yeast, fermentation 120 min, proofing 60 min, 35 °C

0.82 g/100 g (dw) in dough initially, 69% degraded

Whole wheat bread

Baker´s yeast, fermentation 4.5 h, 30 °C

2.0 g/100 g (dw) in flour 0.19 g/100 g (dw) in bread

(Gélinas, McKinnon, & Gagnon, 2016) (Ziegler et al., 2016)

Whole wheat bread

Baker´s yeast, fermentation 90 min, proofing 36 min, 30 °C

2.1 g/100 g (dw) in dough initially, 78% degraded

(Verspreet et al., 2013)

Whole wheat bread

Baker´s yeast, 25 min kneading, 100 min fermentation (temperature not given)

1.5 g/100 g (dw) in flours, 0.80 g/100 g in bread

(Knez et al., 2014)

Whole wheat bread

K. marxianus and 2% (dw) sucrose, fermentation 90 min, proofing 36 min, 30 °C K. marxianus and amyloglucosidase, fermentation 90 min, proofing 36 min, 30 °C

2.0 g/100 (dw) in dough initially >85% degraded after baking 2.0 g/100 (dw) in dough initially >95% degraded after baking

(Struyf et al., 2018)

Whole wheat bread

Baker´s yeast and K. marxianus co-culture, fermentation 180 min, 30 °C

2.3 g/100 g (dw) in dough initially, >95% degraded

Whole Emmer wheat bread

Baker´s yeast, fermentation 120 min, proofing 60 min, 35 °C

1.1 g/100 g (dw) in dough initially, 79% degraded

(Struyf, Laurent, Verspreet, Verstrepen, & Courtin, 2017) (Gélinas et al., 2016)

Whole Khorasan wheat bread

Baker´s yeast, fermentation 120 min, proofing 60 min, 35 °C

1.3 g/100 g (dw) in dough initially, 77% degraded

(Gélinas et al., 2016)

Whole spelt bread

Baker´s yeast, fermentation 4.5 h, 30 °C

1.2 g/100 g (dw) in flour 0.22 g/100 g (dw) in bread

(Ziegler et al., 2016)

Rye flour

Fermentation with a fructan-degrading starter for 6 h (temperature not given)

~4 % (dw) fructan initially, all consumed

(Loponen, 2016)1

Rye bread

Starter culture and Lb. crispatus fructanase, fermentation 120 min, 37 °C

Bread without fructanase 1.4% (dw), Enzyme treated bread 0.15% (dw)

(Loponen et al. 2017)1

Whole rye bread

Commercial sour-dough bread (bread making not described)

5 g/100 g (dw) in flour, 1.9 g/100 g (dw) in bread

Rye-wheat bread (3:7)

Baker´s yeast, 25 min kneading, 100 min fermentation (temperature not given)

2.4 g/100 g (dw) in flours, 1.4 g/100 g in bread

(Andersson, Fransson, Tietjen, & Åman, 2009) (Knez et al., 2014)

Mixed bread: wheat, oats, rye (8:8:5)

Baker´s yeast and Lb. crispatus fructanase, resting 20 min, proofing 45 min, 40 °C

Bread without fructanase 0.34% (dw) Enzyme treated bread 0.17% (dw)

(Loponen et al. 2017)1

Garlic

Incubation with Lb. crispatus fructanase, 50 °C, 5 h

20 g/100 g (ww), 60% degraded

(Loponen et al. 2017)1

Jerusalem artichoke

Incubation with Lb. crispatus fructanase, 50 °C, 5 h

12 g/100 g (ww) initially, 68% degraded

(Loponen et al. 2017)1

Whole wheat bread

1

Data from a patent example.

(Struyf et al., 2018)

Table 4. Reduction of galacto-oligosaccharide content of various solid foods by added enzymes. Enzyme

Substrate

Mortierella vinacea α-gal extract

Soybean and cannola

Energex (Novo Industri), invertase, M. vinacea α-gal extract (1:0.5:1; w w-1)

Reduction by other treatments (whole beans)

Reference

65 % of raff. + stach.

No other treatments

(Slominski, 1994)

Soybean and cannola

100% of raff. + stach.1

No other treatments

(Slominski, 1994)

M. vinacea IBT-3 α-gal extract

Lentil

90% of raff. and 95% of stach.

Crude α-gals of Cladosporium cladosporides, Aspergillus oryzae and A niger

Chickpea

100% of raff. and stach.

78% of raff., 85% of stach. by cooking; 15% of raff. and 29% of stach. by autoclaving 69% of raff. and 75% of stach. by germination, 49% of raff. and 33% of stach. by presoaking-cooking

(Miszkiewicz & Galas, 2000) (Mansour & Khalil, 1998)

Rhizomucor miehei α-gal (recomb.) Crude α-gal of A. niger

Soy bean and kidney bean

100% of raff. and stach.

No other treatments

(Katrolia et al., 2012)

Cowpea

95% of raff. and 82% of stach.

No other treatments

Partially purified Cassia sericea α-gal

Red gram

100% of raff., stach. and verbasc.

55% of raff., 55% of stach. and 33% of verbasc. by soaking; 80% of raff., 87% of stach. and 82% of verbasc. by cooking

(Somiari & Balogh, 1992) (Mulimani & Devendra, 1998)

Crude Cyamopsis tetragonolobus (guar) α-gal

Soybean

90% of raff. and 92% of stach.

80% of raff. and 45% of stach. by soaking; 52% of raff., 21% of stach. by cooking

Penicillium griseoroseum α-gal (free enzyme)

Soybean

39% of raffinose and 100% of stachyose

No other treatments

(Mulimani, Thippeswamy, & Ramalingam, 1997) (Falkoski et al., 2009)

P. griseoroseum α-gal immobilized covalently on silica

Soybean

70% of raffinose and 100% of stachyose

No other treatments

(Falkoski et al., 2009)

Crude A. awamori α-gal

Pinto bean

100% of raff. + stach.

(Song & Chang, 2006)

Crude Cassia sericea α-gal

Jack bean and sword bean accessions Bengal velvet bean accessions

73-84% of raff., 67-91% of stach., 69-84% of verbasc. 79-85% of raff., 95-98% of stach., 82-83% of verbasc.

Black bean Red bean Navy bean

51% of raffinose + stachyose 30% of raff. + stach. 46% of raff. + stach.

10% of raff. + stach. by soaking, 52% by cooking, 58% by autoclaving3 11-57% of raff., 13-51% of stach. and 8-52% of verbasc. by soaking followed by cooking 5-18% of raff., 4-38% of stach. and 4-28% of verbasc. by soaking; 38-42% of raff., 53-62% of stach. and 48-55% of verbasc. by repeated boiling; 40-43% of raff., 53-57% of stach. and 52-54% of verbasc. by autoclaving 61% of raff. + stach. by germination and 33% by soaking 61% of raff. + stach. by germination, 0% by soaking 70% of raff. + stach. by germination; 0% by soaking

Crude Cassia sericea α-gal

ALPHA-GAL (Novozymes Inc.)2 ALPHA-GAL (Novozymes Inc.)2 ALPHA-GAL (Novozymes Inc.)2 1

Reduction by α-gal (flour)

Considerable generation of mellibiose and manninotriose. Enzymatic reaction carried out under sonication in 70% (v/v) ethanol. 3 Preheated before enzyme treatment. 2

(Pugalenthi, Siddhuraju, & Vadivel, 2006) (Janardhanan, Gurumoorthi, & Pugalenthi, 2003)

(Matella et al., 2006) (Matella et al., 2006) (Matella et al., 2006)

Table 5. Reduction of galacto-oligosaccharide content of various foodstuffs through fermentation. Only highest achieved reductions by fermentation are reported. Organism(s) Bifidobacterium breve MB233, Bifidobacterium infantis MB258, Bifidobacterium bifidum MB300

Substrate Soybean (Glycine max)

Form Soy milk

Reduction by fermentation 100% of raff. + 64% of stach.

Reference (Scalabrini, Rossi, Spettoli, & Matteuzzi, 1998)

Natural fermentation

Beans (Phaseolus vulgaris)

Seeds, Flour

100% of raff. + 100% of stach.

(Granito et al., 2002)

Lactobacillus casei, Lactobacillus plantarum

Black beans (Phaseolus vulgaris)

Seeds

88.6% of raff.

(Granito & Álvarez, 2006)

Leuconostoc pseudomesenteroides DSM 20193, Leuconostoc mesenteroides subsp. mesenteroides DSM 20240, Leuconostoc citreum DSM 5577, Weissella cibaria DSM 15878

Faba bean (Vicia faba)

Flour

100% of raff. + 100% of stach. + 100% verb.

(Xu, Wang, et al., 2017)

Leuconostoc mesenteroides DSM 20343

Faba bean (Vicia faba), Soybean (Glycine max) Australian sweet lupin (Lupinus angustifolius) Faba bean (Vicia faba)

Flour

(Xu, Coda, Shi, Katina, & Tenkanen, 2017) (Kaczmarska, Chandra-hioe, Zabaras, Frank, & Arcot, 2017) (Rizzello, 2019)

Flour

Lactobacillus rossiae LB5, Lactobacillus plantarum 1A7, Lactobacillus sanfranciscensis DE9

Lentil (Lens culinaris var. Vulgaris cv. Magda 20) Chickpea (Cicer arietinum), Lentil (Lens culinaris)

100% of raff. + 100% of stach. + 100% verb. 40% of stach. + 29% verb. (279% increase in raff.) 100% of raff. + 73% of stach. + 84% verb. 100% of raff. + 100% of stach.

Lactobacillus plantarum

Soybean (Glycine max)

Natural fermentation, fermentation with yogurt starter YO-MIX (DuPont) Weissella cibaria VTT E-153485, Weissella confusa VTT E-143403, Pediococcus pentosaceus VTT E-153483, Leuconostoc kimchi VTT E-153484 Natural fermentation

Flour Flour

Flour, Sprouted flour Seeds

95% of raff.

(Frias, Díaz, L. Hedley, & Vidal-Valverde, 1996) (Montemurro, Pontonio, Gobbetti, & Giuseppe, 2019)

Enterococcus spp. F09, Enterococcus casseliflavus F05, Lactobacillus sakei Faba bean (Vicia faba) F71; F1410, Lactococcus lactis F55, Leuconostoc mesenteroides I01; I21; I57; I211, Pediococcus spp. I56; Pediococcus pentosaceus F01; F15; F77; F213; I02; I014; I76; I147; I214, Weissella cibaria F16; F110, Weissella koreensis F111; F113; I06; I19; I148; I149 Lactobacillus bulgaricus, Streptococcus thermophilus Soybean (Glycine max)

Flour

68% of raff. + 76% of stach. + 71% (Adeyemo, & Onilude, 2014) verb. 40% of raff. (Verni et al., 2017)

Soy milk

31,5% of stach.

Yogurt starters Yo-Mix 205 LYO (DuPont), FD-DVS ABY-3 Probio-Tec (Christian Hansen)

White kidney beans (Phaseolus vulgaris)

17% of raff. + 31% of stach.

Yogurt starter FD-DVS YC-X11 (Christian Hansen)

Black soybean (Glycine max (L.) Merrill) Drum and oloyin beans (Vigna unguiculata) Soybean (Glycine max)

Broth of germinated seeds Broth

(Omogbai, Ikenebomeh, & Ojeaburu, 2005) (Ziarno, Zaręba, Maciejak, & Veber, 2019)

16% of raff. + 35% of stach.

(Feng, Saw, Lee, & Huang, 2008)

Broth

79% of raff. + 68% of stach.

(Adewumi & Odunfa, 2009)

Soy milk

39% of raff. + 29% of stach.

(Battistini et al., 2018)

Soybean (Glycine max)

Soy milk

100% of raff. + 72% of stach.

(Liu, Li, Yang, Liang, & Wang, 2006)

Lactobacillus plantarum, Lactobacillus fermentum, Pediococcus acidilactici Lactobacillus acidophilus La-5, Bifidobacterium animalis Bb-12, Streptococcus thermophilus Lactobacillus rhamnosus 6013 Kefir starter culture Lyofast TM 036 LV (Clerici Sacco)

Soybean (Glycine max)

Soy milk

100% of raff. + 91% of stach.

(Baú, Garcia, & Ida, 2015)

Lactobacillus curvatus R08, Leuconostoc mesenteriodes JK55

Soybean (Glycine max)

Soy milk

100% of raff. + 100% of stach.

(Yoon & Hwang, 2008)

Lactobacillus fermentum, Lactobacillus plantarum

Cowpea (Vigna sinensis L. var. carilla)

Flour

80% of raff. + 96% of stach.

Natural fermentation

Pigeon pea (Cajanus cajan)

Flour

(Doblado, Frias, Munoz, & VidalValverde, 2003) 89% of raff. + 88% of stach. + 72% (Torres, Frias, Granito, & Vidal-Valverde, verb. 2006)

Table 6. Reduction of galacto-oligosaccharide content of various legume seeds by germination. Legume(s)

Germination time

Temperature

Illumination

Reduction by germination

Reference

Faba bean (Vicia faba)

6 days

20°C

Dark

12% of raff. + 100% of stach. + 100% verb.

(Vidal-Valverde et al., 1998)

Bean (Phaseolus vulgaris L, var. La Granja) Lentil (Lens culinaris L, var. Castellana) Pea (Pisum sativum L, var. Esla)

2, 4, 6 days

20°C

Dark and Light

100% of raff. + 100% of stach. 100% of raff. + 100% of stach 82% of raff. + 100% of stach

(Vidal-Valverde et al., 2002)

Pea (Pisum sativum L, var. Esla)

3, 6 days

20°C

Dark

96% of raff. + 100% of stach. + 100% verb.

(Urbano et al., 2005)

Faba bean (Vicia faba var. Alameda)

0.5, 1, 2, 3, 4, 5, 6, 7, 8, 9 days

20°C

8/24h Light

47% of raff. + 81% of stach. + 100% verb. + 100% ajuc.

(Goyoaga et al., 2011)

Cowpea (Vigna unguiculata) Bean (Phaseolus vulgaris)

1, 2, 3 days

28°C

12/24 h Light

83% of raff. 100% of raff.

(Ribeiro et al., 2011)

Lima bean (Phaseolus lunatus) Pigeon pea (Cajus cajan) African yam beans (Sphenostylis stenocarpa) Jack bean (Canvalia ensiformis)

0.5, 1, 2, 3, 4 days

25°C

8/24 h Light

100% of raff. + 87% of stach. + 100% verb. 100% of raff. + 55% of stach. + 100% verb. 78% of raff. + 72% of stach. + 56% verb. 100% of raff. + 79% of stach. + 100% verb

(Oboh et al., 2000)

Mung bean (Phaseolus aureus)

3 days

r.t. (~25°C)

Dark

100% of raff. + 100% of stach.

(Mubarak, 2005)

Cowpea (Vigna unguiculata) Jack bean (Canvalia ensiformis) Mucuna (Stizolobium niveum) Dolichos (Lablab purpureus) Soybean (Glycine max)

4 days

25°C

Dark, 12/24h Light and Light

87% of raff. + 100% of stach. 95% of raff. + 100% of stach. 100% of raff. + 91% of stach. 100% of raff. + 77% of stach. 69% of raff. + 100% of stach.

(Martín-Cabrejas et al., 2008)

Faba bean (Vicia faba)

3 days

r.t. (~25°C)

Dark

100% of stach.

(Khalil & Mansour, 1995)

Ricebean (Vigna umbellata)

1, 2 days

37°C

Dark

51% of raff. + 75% of stach.

(Kaur & Kawatra, 2000)

Mung bean (Vigna radiata) Pea (Pisum sativum var. Lencolen) Lentil (Lens culinaris var. Giza 9)

3, 5 days

r.t. (~25°C)

Dark

99% of raff. + 99% of stach. 99% of raff. + 99% of stach. 99% of raff. + 99% of stach.

(El-Adawy, Rahma, El-Bedawey, & ElBeltagy, 2003)

Chickpea (Cicer arietinum)

3 days

r.t. (~25°C)

Dark

100% of raff. + 100% of stach.

(El-Adawy, 2002)

Pigeon peas (Cajus cajan)

1, 2, 3 days

25°C

8/24 h Light

100% of raff. + 88% of stach. + 100% verb.

Soybean (Glycine max) Mung bean (Vigna radiata)

1, 2, 3 days

28°C

N/A

100% of raff. + 100% of stach. 100% of raff. + 100% of stach.

(Raja, Agasimani, Varadharajan, & Ram, 2016) (Abdullah, Baldwin, & Minor, 1984)

Soybean (Glycine max) Mung bean (Vigna radiata)

1, 2, 3, 4, 5 days

27°C

Dark

100% of raff. + 99% of stach. 100% of raff. + 100% of stach. + 100% verb.

(Kuo, VanMiddlesworth, & Wolf, 1988)

Mung bean (Vigna radiata) Lentil (Lens culinaris) Chickpea (Cicer arietinum)

1, 2, 3, 4, 5 days

N/A

N/A

100% of raff. + 100% of stach. + 100% verb. 0% of raff. + 81% of stach. + 84% verb. 55% of raff. + 82% of stach. + 62% verb.

(Kadlec, Dostálová, Bernášková, & Skulinová, 2008)

Lupin (Lupinus albus var. multolupa) Black beans (Phaseolus vulgaris) Soybean (Glycine max)

2 days

28°C

Dark

89% of raff. + 96% of stach. 67% of raff. + 65% of stach. 40% of raff. + 77% of stach.

(Donangelo, Trugo, Trugo, & Eggum, 1995)

Red kidney beans (Phaseolus vulgaris) Black-eyed pea (Vigna unguiculata L. Walp.)

2, 4, 6 days

r.t.

Dark

97% of raff. + 96% of stach. 100% of raff. + 100% of stach.

(Labaneiah & Luh, 1981)

a)

b)

c)

d)

e)

f)

Highlights • • •

Many foods containing FODMAP are good sources of dietary fibre and phytochemicals. Their gastrointestinal tolerance can be improved by targeted FODMAP hydrolysis. FODMAP content can be reduced by enzymatic treatment, fermentation or germination.