Low FODMAPs Foodstuffs

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This entry is adapted from the peer-reviewed paper 10.3390/foods12040856

There has been a growing interest in a diet low in fermentable oligosaccharides, disaccharides, monosaccharides, and polyols (FODMAPs) as a promising therapeutic approach to reduce the symptoms associated with irritable bowel syndrome (IBS). Hence, the development of low FODMAPs products is an important challenge for the food industry, and among the various foodstuffs associated with the intake of FODMAPs, cereal-based products represent an issue.

irritable bowel syndrome fermentable carbohydrates functional food

1. Introduction

Irritable bowel syndrome (IBS) is a chronic gastrointestinal disease identified by recurrent abdominal pain associated with defecation together with a change in bowel habits ^[1]. IBS is very common and has a worldwide prevalence of 9% in males and 14% in females ^[2]. Based on the Rome IV criteria, which classifies IBS in four subtypes depending on the predominance of the stool form, the most common (40–60%) subtype is the one with predominance of diarrhea (IBS-D) ^[3]^[4]. The etiology of IBS is still unknown, but it appears to be multifactorial and includes different pathogenic pathways involving impairment of the brain–gut axis, visceral hypersensitivity, alteration of the immune system, derangement of gut microbiome, and psychosocial factors. Because of the high incidence of anxiety and depression in functional disorders ^[5], IBS is associated with decreased quality of life ^[6]^[7] and has a notable impact on healthcare systems ^[8]^[9]^[10]^[11]. The pharmacological therapeutic options for IBS are still unsatisfactory ^[12]; therefore, the interest of physicians and patients for dietary interventions is rising in last years. Some foods are known to be poorly tolerated by patients with IBS ^[13]^[14], and modifications in the intake of fibers and other triggers (i.e., caffeine, alcoholic beverages, and fats) represent a common therapeutic advice for IBS ^[15]^[16]^[17]^[18]^[19]. Furthermore, a gluten-free diet appears to provide an amelioration of symptoms in patients with diarrhea-predominant IBS ^[20]^[21]^[22], although with alternate results ^[23]. More recently, the restriction in the intake of FODMAPs has appeared as a promising therapeutic option in patients with IBS, as supported by an increased body of evidence ^[24]. In Europe, owing to the lack of legislation, very few products with a low FODMAPs labelling are available on the market and, as mentioned before, IBS patients use gluten-free products, generally low in FODMAPs.

However, for IBS patients, gluten elimination is not strictly necessary and not even recommended considering the lacking sensory appeal, structure, and nutritional value ^[25]. Thus, the development of sensorially accepted low FODMAPs breads and cereal- based foods, produced through a careful selection of the raw material as well as considering the fiber inclusion and exploiting the FODMAPs reduction via a bioprocessing approach, is an emerging area of research.

2. FODMAP Classifications

The acronym FODMAPs was coined by Gibson and Shepherd ^[26] and linked to a low FODMAPs diet that has been shown to improve the IBS pathology, as reported by extensive clinical research.

The FODMAPs have common characteristics at the level of metabolic fate (Table 1). In fact, they are poorly absorbed in the small intestine, and then arrive unbroken in the colon, where are rapidly metabolized by the bacterial microflora ^[27]. During colonic fermentation, there is gas production (hydrogen and methane), which leads to an extension of the colon, and a consequent increase of water in the lumen that, finally, can lead to diarrhea.

Table 1. Classification of the fermentable oligo-, di-, mono-saccharides, and polyols (FODMAPs).

Classes	Examples
Oligosaccharides	Fructans (FOS), Galacto-oligosaccharides (GOS)
Polysaccharides	Lactose
Monosaccharides	Fructose
Polyols	Sorbitol, mannitol, xylitol, erythritol, polydextrose, and maltitol

FOS and GOS. The FOS and GOS are the main FODMAPs ingested through diet, and they are widely present in cereals and legumes (wheat, spelt, barley, rice, chickpeas, lentils, peas) and in some vegetables (garlic, onion, cabbage) ^[28]. They are large molecules, composed by oligosaccharides with different degrees of polymerization, which are also based on their natural or enzymatic source. In functional foods manufacturing, FOS and GOS are added for their prebiotic properties but also to exert beneficial actions such as reducing constipation and controlling body weight or as low-calorie sweeteners ^[29] (Figure 1).

Figure 1. Examples of FODMAPs’ chemical structures. (A) Fructans: e.g., inulin composed by fructose units linked β(2-1) glycosidic bonds, with a total polymerization degree according to the origin plant; (B) Galacto-oligosaccharides: e.g., stachyose consisting of sucrose that has an α-D-galactosyl-(1→6)-α-D-galactosyl moiety attached at the 6-position of the glucose; (C) disaccharides: e.g., lactose made up of one unit each of glucose and galactose, joined by β-1, 4 glycosidic linkage.

Lactose. Lactose is the main disaccharide present in mammalian milk and its derivatives; it is formed by galactose and glucose and linked by β(1-4) glycosidic bond. Generally, lactose is digested in the intestine by a lactase enzyme present on the intestinal brush border, releasing two monosaccharides. In patients with lactase deficiency, the lactose reaches the colon unbroken where is metabolized by intestinal microflora and can be classified as a FODMAP ^[30]. Yang et al. ^[31] observed that intestinal gas production was proportional to the amount of lactose ingested, and these symptoms increased in patients with IBS. However, to date, the effects of lactase deficiency on symptoms of irritable bowel syndrome (IBS) are still not well defined ^[32] (Figure 1).

Fructose. The dietary sources of fructose are mainly fruits and honey. In the intestinal lumen, fructose is present as free hexose or following hydrolysis of sucrose and it can included as a FODMAP when it is not equimolar with glucose. This is because of its two-absorption mechanism; by the GLUT5 on the brush border membrane, however this is a low capacity transport, and by GLUT2, which is responsible for carrying both fructose and glucose out of the enterocyte across the basolateral membrane ^[33]. The excess of fructose drives to its malabsorption and colonic metabolism which, through fermentation, can lead to osmotic diarrhea, gas, and bloating ^[34] (Figure 2).

Figure 2. Examples of FODMAPs’ chemical structures. (A) Monosaccharides; (B) polyols.

Polyols. Polyols are sugar alcohols naturally present in some fruits, vegetables, mushrooms, and sugar-free sweeteners; they are formed by catalytic hydrogenation of carbohydrates and in several products, such as chewing gum, candies, and beverages, are used as alternatives to sucrose, yielding fewer calories per gram, low blood glucose response, and protecting against tooth decay ^[35]. Polyol human metabolism goes through a passive diffusion and absorption (about 33%) in the small intestine, with an absorption rate depending on both the individual patient and the molecular size of the polyol ^[36]. To date, it is still unclear if polyol ingestion increases the symptoms of the disease in patients with IBS ^[37]. However, the slow absorption of sorbitol and mannitol leads to their rapid metabolism by the colonic microflora with a consequent increase of luminal water content and production of gas, triggering abdominal symptoms ^[38] (Figure 2).

3. FODMAPs Content in Foods

The management of IBS should take into account the challenge of balance the high increase rates of IBS and the possibility of introducing new foods fully fitting into the low FODMAPs diet, which is an eating practice that allows for improving this pathology ^[39]. FODMAPs are found in a wide variety of foods, such as breads, grains, nuts, legumes, fruits, vegetables, and sweets. An accurate estimate of the FODMAPs content in a food is difficult to do, as a lot also depends on how the foods are cooked, processed, and administered at the same time ^[40]. However, the FODMAPs content levels has been provided by several scientific investigations that deal with this issue and actually, it is possible to differentiate between foods with a high and low content of FODMAPs (Table 2) ^[41].

Table 2. Examples of low and high FODMAP foods, based on the standard serving size.

Food	Low FODMAPs	High FODMAPs
Fruits	Kiwifruit, blueberry, banana, mandarin, orange, passionfruit, grapefruit.	Peaches, apples, pears, watermelon, cherries, mango, apricots.
Vegetables	Carrot, celery, lettuce, eggplant, zucchini, green beans, bok choy.	Asparagus, Brussels sprout, cabbage, fennel, mushrooms, onion, garlic.
Dairy	Brie/camembert cheese, feta cheese, lactose-free milk.	Cow, sheep and goat milk, ice cream, yoghurt, ricotta, cottage.
Grain/cereals	Gluten-free bread/cereal products, sourdough spelt bread, quinoa/rice/corn pasta.	Pasta, wheat bread, biscuits, couscous.
Sweeteners	Maple, rice malt and golden syrups, sucrose.	Honey, high fructose corn syrup, sorbitol, mannitol, xylitol.

Ispiryan et al. ^[25] quantified and characterized FODMAPs in cereals and legumes as wheat substitutes in dietary foods. In particular, legumes, such as peas and broad beans, contained high amounts of GOS (from 4.48 to 4.87 g/100 g dry matter), whereas fructans were absent. Instead, wheat and other cereals (rice, barley) were rich in FOS (from 1.38 to 3.61 g/100 g dry matter). The same authors proved that some pseudo-cereals such as buckwheat were FODMAPs-free, however, contained other non-digestible soluble sugars (fagopyritols) not included in the FODMAPs classes, but their similar implication in IBS syndrome cannot be excluded. In the study reported by Liljebo et al. ^[42], a database was implemented by adding to the nutritional data FODMAPs’ most common food items, in order to make easier the estimation of daily FODMAPs intake, which took place over 4 days using 117 Swedish individuals.

In the beverages, fruits, and vegetables most commonly consumed, fructose was present in grams, whereas the major fructan intake arose from the wheat, rye, fruit, and vegetable consumption. The lactose was derived from the intake of milk and yogurt. The GOS came from bread, both wheat and rye and, finally, the intake of polyols was also derived from fruits. As result of the study, the average daily FODMAPs intake of 19 g was calculated, and the data is in agreement with other studies performed on healthy populations. Although some limitations have to be considered, such as seasonal variation, stage of ripeness, and genetic variation of the analyzed samples, the investigation allowed for recommending guidelines on monitoring the dietary intake of FODMAPs and to have a list of the most common foods, to facilitate their inclusion or exclusion into a Low FODMAPs diet ^[42]^[43]. Updating needs and acquiring database-organized data on FODMAPs content is a challenge that concerns in particular the functional foods sector.

4. Cereal Product Formulations with Low FODMAPs Content for Consumers with IBS

For the targeted development of a low-FODMAPs product, there are specific cut-off levels related to the content of oligosaccharides (fructans and galacto-oligosaccharides), sugar polyols (mannitol and sorbitol), lactose, and fructose in excess of glucose, which should be considered and used as a benchmark ^[40]. These cut-offs have been validated and established based on the findings of clinical studies, considering the typical serving size of food consumed as a singular meal that triggered the symptoms in IBS patients. For grains, legume, nuts, and seeds oligosaccharides (fructan and α-galacto-oligosaccharides), the cut-off value is <0.30 g per serving. For vegetables, fruits, and all other products, the oligosaccharides cut-off is <0.20 g per serving and the same cut-off is true for sorbitol or mannitol, whereas for total polyols it is <0.40 g per serving. When fructose in excess to glucose is the only FODMAP present (for fruit or vegetables), the cut-off is <0.40 g per serving instead when there are other FODMAPs, when the value for fructose in excess to glucose is <0.15 g per serving. Finally, for lactose, the cut-off level is <1.00 g per serving size.

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